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Research Article
Leaf epidermal micromorphology in Aspidistra (Asparagaceae): diversity and taxonomic significance
expand article infoNikolay A. Vislobokov§, Long-Fei Fu|, Yi-Gang Wei|, Maxim S. Nuraliev§
‡ Joint Russian-Vietnamese Tropical Scientific and Technological Center, Hanoi, Vietnam
§ M.V. Lomonosov Moscow State University, Moscow, Russia
| Guangxi Institute of Botany, Guangxi Zhuang Autonomous Region and Chinese Academy of Sciences, Guilin, China
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Abstract

Micromorphological characters of leaf epidermis were investigated in 69 species of Aspidistra using scanning electron microscopy. Sculpture of epidermis varies from smooth to verrucose and rugose in the genus. The abaxial epidermis of some species bears papillae, whereas the adaxial surface uniformly lacks the papillae. Sculpture type of epidermis and density of papillae are generally found to be stable characters at a species level. The infraspecific variation of epidermis sculpture, where present, ranges from smooth to verrucose or from verrucose to rugose. Micromorphological characters of leaf epidermis are shown to have potential taxonomic significance in Aspidistra; in combination with the type of shoot structure, they allow to subdivide the species into 13 groups. The groups are largely incongruent with floral morphological traits. An identification key to the studied species of Aspidistra based on vegetative characters (gross leaf and shoot morphology and characters of leaf epidermis) is presented.

Keywords

Aspidistra, epidermis, identification key, papillae, SEM

Introduction

Aspidistra Ker Gawl., belonging to the family Asparagaceae, is a large genus of herbaceous plants which inhabits tropical and subtropical forests of Asia. In our estimate, the genus comprises about 200 species. Aspidistra is remarkable for its extremely diverse flower morphology (Tillich 2005, 2008, 2014; Averyanov and Tillich 2012; Tillich et al. 2017; Tillich and Averyanov 2018). Floral characters are most important in taxonomy of Aspidistra, whereas vegetative characters are rarely used for species identification: most of the species have similar habit and are hardly distinguishable without flowers. The majority of representatives of Aspidistra are characterized by creeping rhizome without aerial shoots. Only a few species have erect stem (e.g. A. erecta Yan Liu & C.I Peng and A. globosa Vislobokov & Nuraliev), representing a group easily recognizable by vegetative morphology (Vislobokov et al. 2016). Another non-floral character that was shown to have taxonomic significance in Aspidistra is the distribution of foliage leaves along the shoot (De Wilde and Vogel 2006; Averyanov and Tillich 2014). Shoots of Aspidistra consist of repeatedly developing elementary shoots, each elementary shoot bearing several cataphylls followed by one to several foliage leaves (Vislobokov et al. 2014, 2017). The species of Aspidistra can be divided into two groups: the first group is characterized by solitary leaves (i.e., one foliage leaf per elementary shoot), and in the second group the leaves are arranged in tufts (i.e., 3–5 foliage leaves per elementary shoot). Additionally, these groups of species differ in the gross morphology of leaf. In most species of the first group, the leaf is divided into petiole and blade (e.g. A. arnautovii Tillich, A. formosa (Tillich) Aver. & Tillich, A. subrotata Y.Wan & C.C.Huang), with blade of various shape. By contrast, all species of the second group have narrowly elliptic or linear leaves lacking a petiole but gradually tapering towards base (e.g. A. carnosa Tillich, A. hainanensis W.Y.Chun & F.C.How, A. viridiflora Vislobokov & Nuraliev). The second group is much smaller with respect to species number than the first one.

Despite the usefulness of the vegetative characters of Aspidistra outlined above, they are far from being enough for identification to the species level, because numerous species often share the same combination of these characters. Thus, the precise identification of Aspidistra in non-flowering condition in most cases is impossible at the current state of knowledge. At the same time, identification of sterile plants of Aspidistra appears to be highly demandable due to several features of reproductive biology of this genus. The flowers in Aspidistra are usually developed at the ground level, often hidden by leaf litter, and their search requires special efforts (Tillich 2005). The field recognition of species of Aspidistra is also complicated by their common sympatric occurrence: three or four (and up to six) species are often recorded in a given forest, where they sometimes grow side by side forming mixed populations (Nuraliev et al. 2017). Moreover, the flowering takes place only in a particular season, which differs among the species, so that only a part of individuals of the genus (if any) are usually observed to produce flowers in a given forest. A widely used technique of specimen identification in Aspidistra is collecting sterile living material and obtaining the flowers under cultivation (Averyanov and Tillich 2014, 2015; Vislobokov et al. 2019b). However, this method requires a preliminary estimation of the number of the species inhabiting a given area.

Micromorphological characters, including those of vegetative organs, sometimes appear sufficiently diverse to serve as a useful instrument for taxonomy and species identification. This approach has already been successfully applied for Dracaena Vand. ex L., another genus of Asparagaceae (Klimko et al. 2018), as well as for certain genera of Caryophyllaceae, Lamiaceae and Myrtaceae (Haron and Moore 1996; Mostafavi et al. 2013; Krawczyk and Głowacka 2015). To date, micromorphology has never been investigated in Aspidistra. In the present study, we investigated micromorphological characters of leaf epidermis in this genus. Our goals were (1) to evaluate diversity of adaxial and abaxial leaf epidermis in Aspidistra including cell sculpture and density of papillae; (2) to determine infraspecific variation of these characters; (3) to analyze taxonomic significance of characters of leaf epidermis by delineating species groups on the basis of these characters; (4) to compile an identification key to the studied species of Aspidistra based on vegetative features, including leaf and shoot morphology and the characters of leaf epidermis.

Materials and methods

Specimens

Fully developed foliage leaves were collected from living plants of Aspidistra found in nature (during fieldwork in China and Vietnam) as well as cultivated in the Botanical Garden Munich-Nymphenburg (BGMN), the Botanical Institute of the Russian Academy of Sciences (BIN), the Main Botanical Garden of the Russian Academy of Sciences (MBG) and the Singapore Botanic Gardens (SBG) (Appendix 1). The leaves were fixed and stored in 70% ethanol. All the studied specimens possessed floral material, and identification of the plants used in this study was verified by investigation of floral structure. In total, 113 specimens representing 69 species of Aspidistra were involved in the study. Of them, 45 specimens represent type material (including types and paratypes). Each species was represented by 1 to 8 specimens, and a total of 22 species (ca. 32%) were represented by two or more specimens.

Scanning electron microscopy (SEM)

For SEM, a single fragment ca. 5×5 mm was cut out from the leaf blade by a razor blade for each specimen. The fragment was taken from the central part of the leaf blade (equidistant from petiole/leaf base and leaf apex), equidistantly from midvein and leaf margin, between secondary veins. The dissected material was transferred from 70% ethanol to 100% acetone via 80% and 96% ethanol followed by an 1: 1 mixture of ethanol (96%) and acetone (100%). The material was critical-point dried using an HCP-2 critical point dryer (Hitachi, Japan). Dried samples were divided in two equal parts by a razor blade, which then were mounted onto stubs with different sides exposed, using double-sided sticky tape. The mounted specimens were coated with gold using an Eiko IB-3 ion-coater (Eiko Engineering, Japan) and observed using a CamScan 4DV (CamScan, UK) scanning electron microscope at Moscow State University.

Morphological traits

The following traits of leaf epidermis were investigated: (1) size and shape of epidermal cells; (2) fine relief of the outer periclinal cell wall: micro-sculpture of epidermis surface; and (3) curvature of outer periclinal wall: presence and density of papillae on epidermis. Size of epidermal cells and density of stomata were measured once for each specimen. Density of papillae was measured by counting number of papillae within a frame 100×100 µm in at least two repeats in each specimen. Standard terminology of surface sculpturing patterns mainly follows Barthlott (1981).

The identification key was compiled on the basis of original data on leaf micromorphology and data on gross vegetative morphology available from Liang and Tamura (2000), Li (2004) and the species protologues.

Results

Diversity of micromorphological traits

Leaf epidermis of examined species of Aspidistra consists of elongated tetragonal cells 60–160 µm long and 10–40 µm wide with straight boundaries. The leaves are amphistomatic. Stomata are of anomocytic type. Density of stomata is 50–170 per 1 mm2 on abaxial surface, and very low on adaxial side (less than 10 per 1 mm2). Guard cells are 25–40 µm long and 5–10 µm wide.

Epidermis surface is smooth or sculptured to various degrees (Figs 14). Within the observed variation, we recognize two types of epidermis sculpture: verrucose and rugose. Verrucose surface bears rough irregularities, short wide ridges or projections (e.g. Figs 2e, j, k, o, 3q, r). Rugose surface has numerous fine narrow tortuous folds (e.g. Figs 3e-g, 4m).

Figure 1. 

SEM images of abaxial leaf epidermis of Aspidistra; morphological groups I (a–g), II (h–m) and III (n–t) (partly). a A. graminifolia b A. hainanensis (s.n.) c A. linearifolia d A. oviflora (13394) e A. triradiata f A. viridiflora g A. yingjiangensis h A. carnosa i A. cylindrica j A. hainanensis (11/1394) k A. longifolia l A. oviflora (2018.14340.01) m A. larutensis n A. atroviolacea o A. clausa p A. claviformis q A. dolichanthera (2016.12354.01) r A. erecta s A. jingxiensis t A. lurida. Scale bars: 30 µm.

Epidermis of about a half of the studied specimens is smooth on both surfaces. In the other specimens, the adaxial and abaxial epidermis is either uniformly or differently micro-ornamented (or one of the surfaces is smooth). Usually the sculpture is pronounced to a greater extent on the abaxial surface than on the adaxial one. Verrucose sculpture, if present, is usually found on both sides, or only abaxially with smooth adaxial epidermis. Rugose epidermis is usually expressed on both leaf sides or rarely only on the abaxial side, with the adaxial side being verrucose. Thus, only the abaxial epidermis is illustrated (Figs 14).

Figure 2. 

SEM images of abaxial leaf epidermis of Aspidistra; morphological groups III (a–c) (partly) and IV (d–t). a A. petiolata b A. renatae c A. sessiliflora d A. basalis e A. lateralis f A. medusa g A. typica h A. connata (V/0490) i A. bella j A. erosa (JLS2972) k A. globosa l A. gracilis m A. laotica (20122018) n A. mirostigma o A. phanluongii (2015.11347.01) p A. sarcantha (JLS2962) q A. subrotata (2015.11350.01) r A. sutepensis s A. truongii (2013/2461) t A. vietnamensis. Scale bars: 30 µm.

Adaxial epidermis of foliage leaves of all studied specimens is uniformly epapillate. Abaxial epidermis of about a half of the studied specimens bears papillae (e.g. Figs 3o, 4n, s). Papillae are hemispherical, 10–30 µm in diameter, with one to several of them per epidermal cell. Density of papillae varies from 1 to 45.5 papillae per 0.01 mm2. We recognize three categories of papillae density: low, 1–3.5 papillae per 0.01 mm2; medium, 4–7.5 papillae per 0.01 mm2; high, 8–45.5 papillae per 0.01 mm2.

Additionally, we have found that shape and density of papillae on the secondary veins (not employed in the main part of our study) is different in some specimens from those of the epidermis located between the secondary veins.

Figure 3. 

SEM images of abaxial leaf epidermis of Aspidistra; morphological groups V (a–g), VI (h–l, o), VII (m, n, p–r), VIII (s) and IX (t) (partly). a A. erosa (JLS2906) b A. locii (86-169) c A. lubae d A. xuansonensis e A. corniculata f A. foliosa (97/2360) g A. multiflora h A. fungilliformis (2016.12350.02) i A. geastrum j A. longipetala k A. papillata l A. tillichiana m A. connata (97/2358) n A. semiaperta o A. bicolor p A. clausa q A. opaca (18035) r A. subrotata (A.s.5) s A. minor t A. hekouensis. Scale bars: 30 µm.

The main results of investigation of each species (epidermis sculpture and the presence and density of papillae) are presented in Appendix 1.

Infraspecific variation

Size and shape of epidermal cells of investigated species does not reveal any species-specific pattern: their infraspecific variation is nearly as broad as interspecific variation.

The micro-sculpture of abaxial and adaxial epidermis is, in contrast, generally constant (fixed) at a species level. These traits show stability in at least 16 out of 22 species of Aspidistra represented by two or more specimens in the present study. We found that only in several species the sculpture of at least one leaf side is variable; it varies either between smooth and verrucose, or between verrucose and rugose. We have not observed any species with variation between smooth and rugose sculpture. For example, in two investigated specimens of A. arnautovii adaxial epidermis is verrucose, whereas in the other three specimens (Fig. 4g) the epidermis is smooth (Appendix 1, group X). Epidermis sculpture of A. formosa also varies from verrucose to rugose at adaxial and abaxial surface (Fig. 4r). Finally, two studied specimens of A. erosa Aver., Tillich, T.A.Le & K.S.Nguyen have verrucose adaxial surface but differ in having rugose vs. verrucose surface of abaxial epidermis (Figs 2j, 3a).

Figure 4. 

SEM images of abaxial leaf epidermis of Aspidistra morphological groups IX (a–f) (partly), X (g–l), XI (m), XII (n–q) and XIII (r–t). a A. longanensis b A. lutea (96/3126) c A. sinensis d A. stricta e A. subrotata (20121895) f A. superba g A. arnautovii (18566) h A. connata (96/3119) i A. nutans j A. subrotata (JLS2989) k A. opaca (2013/2460W) l A. subrotata (04/1769) m A. zinaidae n A. bogneri (9311) o A. grandiflora p A. letreae q A. magnifica r A. formosa (2015.11376.01) s A. jiewhoei (JLS1218) t A. marasmioides (2015.11354.01). Scale bars: 30 µm.

Presence and density of papillae is also stable in 16 out of 22 species of Aspidistra represented by two or more specimens. Density of papillae on abaxial epidermis varies only slightly within some species. Appreciable variation was found in A. arnautovii (4–7 papillae per 0.01 mm2; Fig. 4g), A. bogneri (38–45.5 papillae per 0.01 mm2; Fig. 4n), A. lutea Tillich (4–6 papillae per 0.01 mm2; Fig. 4b) and A. opaca Tillich (4–5.5 papillae per 0.01 mm2; Figs 3q, 4k); nevertheless, each of these species fits a single category of papillae density (low, medium or high) proposed above. The most significant variation of this feature was found in A. connata Tillich (0–5 papillae per 0.01 mm2), A. hainanensis (0–1.5 papillae per 0.01 mm2; Figs 1b, j), A. oviflora Aver. & Tillich (0–2.5 papillae per 0.01 mm2; Fig. 1d, l) and A. subrotata (0–6 papillae per 0.01 mm2; Fig. 2q, 3r, 4e); they are categorized as showing variation from absence of papillae to low or medium density of papillae.

Discussion

Combinations of vegetative characters found in Aspidistra

We built a space of logical possibilities for all the studied specimens with regard to the following characters of vegetative morphology: type of shoot, sculpture of adaxial and abaxial epidermis, and density (and presence) of papillae. The specimens showed 23 combinations of these traits. Considering infraspecific variation of some traits, we combined the studied specimens of Aspidistra into 13 groups (Appendix 1) in order to make specimens of the same species belong to one group. This method allowed categorizing specimens of 62 species, whereas 7 species (A. clausa Vislobokov, A. connata, A. erosa, A. hainanensis, A. opaca, A. oviflora, A. subrotata) showed too high variation of traits so that specimens of each species got into several groups. The brief description of these groups is presented in Table 1.

Table 1.

Groups of the examined specimens of Aspidistra recognized here, and traits on which the groups are based.

Group Type of shoot (leaves solitary/tufted) Sculpture of adaxial epidermis Sculpture of abaxial epidermis Density of papillae on abaxial epidermis
I tufted smooth/verrucose smooth/verrucose no papillae
II tufted smooth smooth/verrucose low
III solitary smooth/verrucose smooth no papillae
IV solitary smooth/verrucose verrucose no papillae
V solitary verrucose/rugose rugose no papillae
VI solitary smooth/verrucose smooth low
VII solitary smooth/verrucose verrucose low
VIII solitary rugose rugose low
IX solitary smooth smooth medium
X solitary smooth/verrucose verrucose medium
XI solitary rugose rugose medium
XII solitary smooth smooth high
XIII solitary verrucose/rugose verrucose/rugose high

Some species possess a unique combination of traits, e.g. Aspidistra minor Vislobokov, Nuraliev & M.S.Romanov (Fig. 3s, group VIII) is readily distinguishable from all other studied species by leaf epidermis finely rugose on both sides bearing abaxially papillae of low density. Aspidistra zinaidae Aver. & Tillich (Fig. 4m, group XI) likewise possesses a unique set of traits, which is similar to that of A. minor and differs in medium density of papillae.

We recognized no correlation between the morphological groups of species outlined above and geographical distribution of the species.

The availability of recognition of the morphological groups indicates that the characters under study show an infraspecific variation that is narrow enough, and the interspecific diversity that is broad enough to be applied to taxonomy for most of the studied species of Aspidistra. In other words, the characters possess a taxonomic signal. The identification key provided below is a reflection of this conclusion.

Correlations between leaf micromorphology and floral structure

Most of the groups of species outlined here on the basis of vegetative characters do not show any correlation with floral traits. We were able to recognize only several cases of such correlation, which are addressed below.

Aspidistra mirostigma Tillich & Škorničk., A. phanluongii Vislobokov and A. sarcantha Aver., Tillich, T.A.Le & K.S.Nguyen are similar in floral groundplan and shape: they share trimerous flowers with urceolate perigone, short style and wide stigma with its margin adjoined to the wall of perigone tube (Vislobokov et al. 2013; Leong-Škorničková et al. 2014; Averyanov et al. 2019). These species are demonstrated here to share epapillate leaf epidermis with verrucose sculpture at adaxial and abaxial surface, all belonging to group IV (Fig. 2n, o, p). The micromorphological features are thus in concordance with floral features in this group of species. At the same time, group IV comprises 13 more species, and the floral diversity of the entire group is remarkable high.

Aspidistra atroviolacea Tillich and A. renatae Bräuchler (treated as A. atroviolacea var. renatae (Bräuchler) Tillich & Aver. by Tillich and Averyanov 2018) are similar in having dark violet campanulate perigone and mushroom-shaped pistil (i.e. with slender style and hemispherical stigma) (Bräuchler and Ngoc 2005; Tillich 2005). Both species have epapillate smooth leaf epidermis (Figs 1n, 2b; belonging to group III), again in concordance with the floral features.

A group of five species, A. corniculata Vislobokov, A. erosa, A. foliosa Tillich, A. lubae Aver. & Tillich and A. multiflora Aver. & Tillich, shares trimerous flowers with mostly reddish-purple campanulate perigone and mostly white mushroom-shaped pistil (Tillich 2005; Averyanov and Tillich 2014, 2015; Averyanov et al. 2019; Vislobokov et al. 2019a). This group is uniformly characterized by finely rugose surface of abaxial leaf epidermis and absence of papillae (Figs 3a, c, e, f, g; group V). On the other hand, A. locii Arnautov & Bogner (Fig. 3b, group V) and A. xuansonensis Vislobokov (Fig. 3d; group V) have the same micromorphological traits, but possess distinctly different flowers.

Taxonomically uncertain groups of species in Aspidistra in the light of micromorphological data

The general stability of the micromorphological characters at the species level demonstrated here in Aspidistra allows to discuss taxonomy of complicated groups of species with employment of the newly obtained data.

Representatives of Aspidistra with tufted leaves (i.e., with several foliage leaves per elementary shoot) were considered to form a group of closely related species (De Wilde and Vogel 2006; Tillich and Averyanov 2012). Various authors proposed different taxonomic decisions to accommodate the diversity of plants with this morphology. The entire group was regarded as a single variable species A. longifolia Hook.f. s.l. by Phonsena and De Wilde (2010). Tillich and Averyanov (2012), in contrast, outlined the SE Asian part of this group as A. hainanensis species complex comprising several species (and excluded A. longifolia s.str. decribed from Assam, India from this complex). Here we follow the latter viewpoint, as it describes better the floral variation of these plants. Within our study, the specimens of Aspidistra with tufted leaves form two morphological groups (group I and II) which differ from each other in the presence of papillae on leaf epidermis (absence vs. presence with low density). The leaf epidermis of all these species is usually smooth but slightly tuberous in some cases. Although both characters vary within A. hainanensis species complex, we consider the variation not to be very significant for species delimitation, because it does not exceed the range of infraspecific variation found in some other species (e.g. A. arnautovii and A. subrotata). Thus, our data do not contradict the idea of phylogenetic closeness of these species.

Several other taxa with uncertain boundaries form a group here referred to as A. subrotata species complex. It includes A. subrotata with several described infraspecific taxa and A. connata with two proposed varieties. Aspidistra connata was recently suggested to be treated as a synonym of A. subrotata, as the absence of any considerable differences in their floral structure was shown during investigation of extensive material (Averyanov et al. 2018). Aspidistra subrotata is one of the most widely distributed species of the genus: it was originally described from China (Wan and Huang 1987), and subsequently reported from numerous localities in Vietnam (Tillich 2005, 2014), Thailand (Phonsena and De Wilde 2010) and Laos (Averyanov and Tillich 2017). Aspidistra connata is also known from China (Xu et al. 2010) and Vietnam (Tillich 2005; Leong-Škorničková et al. 2014). Both species inhabit diverse habitats and show extremely high diversity in size of flowers and leaves, shape of the leaf blade, and shape and coloration of the stigma (Averyanov and Tillich 2017). In the present study, A. subrotata and A. connata are expediently treated as distinct species in order to compare their micromorphological characters. Eight specimens of A. subrotata and four specimens of A. connata were investigated. We demonstrate that both species show very high diversity of leaf micromorphology. In both species, sculpture of epidermis varies between smooth and verrucose (but never rugose) adaxially as well as abaxially, and the abaxial side varies from being completely epapillate to having medium density of papillae. Accordingly, specimens of each species fall into several morphological groups (A. subrotata – IV, VI, VIII, IX; A. connata – IV, VI, IX). Thus, features of leaf micromorphology do not provide any clues for delimitation of A. subrotata complex; on the other hand, they do not contradict the idea of distinctness of A. subrotata and A. connata, because the variation found in each species is higher than the variation found in most other species of Aspidistra.

Key for identification of the studied species of Aspidistra based on epidermis micromorphology and gross vegetative morphology

1 Leaves grouped on shoot by 3–5 (3–5 foliage leaves per elementary shoot), sessile; blade narrowly elliptic to linear, 1–5 cm wide, 15–50 times as long as wide 2
Leaves solitary (one leaf per elementary shoot), petiolate or sessile; blade of various shape 6
2 Adaxial epidermis epapillate; abaxial epidermis with sparse papillae (papillae density low: 1–3.5 papillae per 0.01 mm2) 3
Adaxial and abaxial epidermis epapillate 4
3 Epidermis smooth adaxially, verrucose abaxially A. larutensis
Epidermis smooth on both sides A. carnosa , A. hainanensis, A. longifolia, A. oviflora
4(2) Adaxial and abaxial epidermis smooth A. graminifolia , A. hainanensis, A. linearifolia, A. oviflora, A. triradiata
Epidermis verrucose at least on one side 5
5 Epidermis smooth adaxially, verrucose abaxially A. viridiflora
Epidermis verrucose on both sides A. yingjiangensis
6(1) Adaxial and abaxial epidermis smooth and epapillate; leaf petiolate 7
Epidermis sculptured (verrucose or rugose) or papillate at least on one side; leaf petiolate or sessile 9
7 Plant with aerial erect to ascending stem ca. 50 cm high A. erecta
Plant without aerial stem 8
8 Blade narrowly lanceolate to narrowly elliptic, 1.5–4.5 cm wide A. atroviolacea , A. clausa, A. renatae
Blade ovate to elliptic, 5–15 cm wide A. claviformis , A. dolichanthera, A. jingxiensis, A. lurida, A. petiolata, A. sessiliflora
9(6) Adaxial and abaxial epidermis epapillate 10
Adaxial epidermis epapillate, abaxial epidermis papillate 23
10 Epidermis verrucose at least on one side (and never rugose) 11
Epidermis finely rugose at least on one side 18
11 Plant with erect stem 12
Plant without erect stem 14
12 Aerial stem up to 50 cm high A. globosa
Aerial stem 3–20 cm high 13
13 Aerial stem 3–5 cm high, blade 8–16 cm long A. laotica
Aerial stem ca. 20 cm high, blade 20–25 cm long A. lateralis
14(11) Blade narrowly elliptic to narrowly lanceolate, 8–20 times as long as wide 15
Blade elliptic to ovate, 2–7 times as long as wide 16
15 Petiole 3–5 cm long A. basalis
Petiole 15–32 cm long A. erosa , A. gracilis, A. subrotata var. angustifolia
16(14) Epidermis verrucose on both sides A. bella , A. mirostigma, A. phanluongii, A. sarcantha, A. subrotata, A. sutepensis, A. truongii, A. vietnamensis
Epidermis verrucose on one side, smooth on the other side 17
17 Petiole longer than blade A. medusa
Petiole equal to or shorter than blade A. connata , A. typica
18(10) Epidermis finely rugose on both sides 19
Epidermis verrucose adaxially, finely rugose abaxially 20
19 Blade 1.5–3.7 cm wide A. corniculata , A. foliosa
Blade 4–10 cm wide A. multiflora
20(18) Blade elliptic, 5–11 cm wide A. locii , A. xuansonensis
Blade lanceolate, 1.5–5 cm wide 21
21 Blade equal to or insignificantly longer than petiole A. erosa
Blade 2–10 times as long as petiole 22
22 Blade 12–20 cm long, 4–6 times as long as wide A. lubae var. lubae
Blade 20–35 cm long, 8–13 times as long as wide A. lubae var. lancifolia
23(9) Density of papillae on abaxial epidermis low (1–3.5 papillae per 0.01 mm2) 24
Density of papillae on abaxial epidermis medium to high (4–45.5 papillae per 0.01 mm2) 26
24 Epidermis finely rugose on both sides A. minor
Epidermis smooth or verrucose on both sides 25
25 Epidermis smooth on both sides A. fungilliformis , A. geastrum, A. longipetala, A. papillata, A. tillichiana var. latifolia
Epidermis verrucose at least on one side A. bicolor , A. clausa, A. connata, A. opaca, A. semiaperta, A. subrotata
26(23) Density of papillae on abaxial epidermis medium (4–7.5 papillae per 0.01 mm2) 27
Density of papillae on abaxial epidermis high (8–45.5 papillae per 0.01 mm2) 30
27 Epidermis finely rugose on both sides A. zinaidae
Epidermis smooth or verrucose on both sides 28
28 Epidermis verrucose at least on one side A. arnautovii , A. connata, A. nutans, A. opaca, A. subrotata
Epidermis smooth on both sides 29
29 Petiole 2–5 cm long, blade 3–7 times as long as petiole A. lutea , A. sinensis
Petiole 9–28 cm long, blade equal to or insignificantly longer than petiole A. hekouensis , A. longanensis, A. stricta, A. subrotata, A. superba
30(26) Epidermis finely rugose (rarely verrucose) on both sides 31
Epidermis smooth on both sides 33
31 Rhizome with very short internodes (foliage leaves crowded); blade 20–30 × 8.5–13 cm A. jiewhoei
Rhizome with long internodes (foliage leaves spaced 8–25 mm apart); blade 10–17 × 5–8 cm 32
32 Petiole 10–15 cm long, blade 10–12 × 5 cm; epidermis finely rugose on both sides A. marasmioides
Petiole 15–20 cm long, blade 14–17 × 7–8 cm; epidermis finely rugose or verrucose at least on one side A. formosa
33(30) Blade narrowly lanceolate, 1.5–3 cm wide, 23–30 times as long as wide A. letreae
Blade lanceolate, elliptic or ovate, 5–14 cm wide, 6–9 times as long as wide 34
34 Petiole absent or inconspicuous A. bogneri
Petiole distinctly present, usually 30 cm long or longer A. grandiflora, A. magnifica

Conclusions

Micromorphological characters of leaf epidermis show sufficiently high diversity in the genus Aspidistra, and relatively low infraspecific variation in most of its species. The following variable characters are recognized: sculpture of adaxial and abaxial epidermis (smooth, verrucose and rugose) and the presence and density of papillae at abaxial side of leaf (absent, with low, medium and high density). Combined with characters of gross vegetative morphology, they allow recognition of 13 basic types of vegetative morphology in Aspidistra. We constructed an identification key for species of Aspidistra in sterile condition on the basis of the newly obtained micromorphological data and earlier known macromorphological traits. The key allows to identify a species to a group containing one to eight species. The results demonstrate considerable taxonomic significance of micromorphological features in Aspidistra.

Acknowledgements

The authors are grateful to the staff of Botanical Garden Munich-Nymphenburg and personally to Andreas Gröger, staff of the Botanical Institute of the Russian Academy of Sciences and personally to Leonid Averyanov, staff of the Main Botanical Garden of the Russian Academy of Sciences and personally to Mikhail Romanov, staff of Singapore Botanic Gardens and personally to Jana Leong-Škorničková for the opportunity to get material from living collections. The work of N.A. Vislobokov and M.S. Nuraliev was carried out as part of the Scientific Project of the State Order of the Government of Russian Federation to Lomonosov Moscow State University No. 121032500082-2. The reported study was funded by RFBR, project number 18-34-20135 and by RFBR and VAST, project number 21-54-54011.

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Appendix 1

Table A1.

Species and specimens of Aspidistra examined, and traits of vegetative morphology. The species are arranged according to their belonging to the morphological groups, and in the alphabetical order within the groups. Note that some species are represented in more than one group.

Species Living specimens studied Herbarium voucher Country of origin Type of shoot (leaves solitary / tufted) Sculpture of adaxial epidermis Sculpture of abaxial epidermis Density of papillae distribution on abaxial epidermis** Group
Greenhouse hosting specimen* Garden accession number; field collector’s number (if differs from that of herbarium voucher)
A. graminifolia BIN 1285 Averyanov AL 84 (isotype, MW: MW0751740) Vietnam tufted smooth smooth no papillae I
A. hainanensis BIN s.n. - unknown tufted smooth smooth no papillae
A. linearifolia BGMN 2011/0980; Joschko s.n. - unknown tufted smooth smooth no papillae
A. oviflora MBG 2013.12433.01 Vislobokov 13062 (MW: MW0735044) Vietnam tufted smooth smooth no papillae
A. oviflora BIN 13394; Maisak TM1052 Averyanov et al. CPC5425 (isotype, LE: LE01050400) Vietnam tufted smooth smooth no papillae
A. triradiata MBG 2016.12342.01 Vislobokov et al. G30 (MW: MW0753785) China tufted smooth smooth no papillae
A. viridiflora MBG 2015.11381.01 Nuraliev et al. 1280 (holotype, MW: MW0754789) Vietnam tufted smooth verrucose no papillae
A. yingjiangensis BIN 251964 - unknown tufted verrucose verrucose no papillae
A. carnosa BGMN 96/3122W; Arnautov 96-102 Tillich 4476 (holotype, M: M0213536) Vietnam tufted smooth smooth low II
A. cylindrica MBG 2015.11382.01 Kuznetsov et al. 1357 (holotype, MW: MW0595646) Vietnam tufted smooth smooth low
A. hainanensis BGMN 11/1394 Tillich 5717 (M: MSB159621) unknown tufted smooth smooth low
A. longifolia BGMN 15/1593 - unknown tufted smooth smooth low
A. oviflora MBG 2018.14340.01 - unknown tufted smooth smooth low
BIN 14386 Averyanov et al. CPC7491 (LE: LE01050072) Vietnam tufted smooth smooth low
A. larutensis BGMN s.n. - unknown tufted smooth verrucose low
A. atroviolacea BGMN 97/2363 Bogner 2309 (paratype, M: M0213530) Vietnam solitary smooth smooth no papillae III
A. clausa MBG 2014.12431.01 Vislobokov 14097 (holotype, MW: MW0595637) Vietnam solitary smooth smooth no papillae
A. claviformis MBG 2016.12351.01 Vislobokov et al. G71 (MW: MW0753784) China solitary smooth smooth no papillae
A. connata BGMN V/0490 - unknown solitary verrucose smooth no papillae
A. dolichanthera MBG 2016.12354.01 Vislobokov et al. G74 (MW: MW0753743) China solitary smooth smooth no papillae
A. dolichanthera BIN s.n. Averyanov CBL1675 (LE: LE01054609) Vietnam solitary smooth smooth no papillae III
A. erecta MBG 2016.12349.01 Vislobokov et al. G61 (MW: MW0753774) China solitary smooth smooth no papillae
A. jingxiensis MBG 2016.12348.01 Vislobokov et al. G51 (MW: MW0753783) China solitary smooth smooth no papillae
A. lurida BIN 2225 s.coll., s.n. (LE: LE01050063) unknown solitary smooth smooth no papillae
A. petiolata SBG 20121925; Leong-Škorničková JLS1622 - Vietnam solitary smooth smooth no papillae
A. renatae BGMN 04/1772 Brauchler et al. 3000 (holotype, M: M0243611) Vietnam solitary smooth smooth no papillae
A. sessiliflora BIN 14448 Averyanov AL271 (holotype, LE: LE01050440) China solitary smooth smooth no papillae
A. basalis BGMN 2011/1397 Tillich 5720 (holotype, M: MSB159619) China solitary smooth verrucose no papillae IV
A. bella MBG 2019.14670 Averyanov et al. CPC7484 (paratype, LE: LE01042157) Vietnam solitary verrucose verrucose no papillae
A. erosa SBG Leong-Škorničková JLS2972 - unknown solitary verrucose verrucose no papillae
A. globosa from nature - Kuznetsov et al. 1444 (paratype, MW: MW0595640) Vietnam solitary verrucose verrucose no papillae
A. gracilis BGMN 2011/1395 Tillich 5718 (holotype, M: MSB159618) China solitary verrucose verrucose no papillae
A. laotica SBG 20122018 Leong-Škorničková et al. JLS1802 (SING: 0192256) Laos solitary verrucose verrucose no papillae
BIN 1311(1313) Averyanov LA-VN554 (holotype, LE: LE01032172) Laos solitary verrucose verrucose no papillae
A. lateralis BGMN 97/2382; Bogner 2492 Tillich 4361 (holotype, M: MSB004977) Vietnam solitary smooth verrucose no papillae
A. medusa SBG Leong-Škorničková JLS3096 - Laos solitary smooth verrucose no papillae
A. mirostigma SBG Leong-Škorničková JLS1571 Leong-Škorničková et al. JLS-1571 (holotype SING) Vietnam solitary verrucose verrucose no papillae
A. phanluongii MBG 2015.11347.01 Nuraliev 874 (MW: MW0735057) Vietnam solitary verrucose verrucose no papillae
from nature - Vislobokov M0211 (paratype, MW: MW0591735) Vietnam solitary verrucose verrucose no papillae
A. sarcantha SBG Leong-Škorničková JLS2914 - Vietnam solitary verrucose verrucose no papillae
SBG JLS2962 Leong-Škorničková et al. JLS2962 (SING: 0240186) Vietnam solitary verrucose verrucose no papillae
A. subrotata var. subrotata BGMN 97/2376 II Tillich 4461 (M: M0213561) Vietnam solitary verrucose verrucose no papillae
MBG 2015.11350.01 Vislobokov 13067 (MW: MW0735071) Vietnam solitary verrucose verrucose no papillae IV
A. subrotata var. angustifolia MBG 2015.11365.01 Vislobokov 13097 (MW: MW0735079) Vietnam solitary verrucose verrucose no papillae IV
A. sutepensis BGMN 05/2338 Tillich 5081 (M: MSB126218) Thailand solitary verrucose verrucose no papillae
A. truongii BGMN 2013/2461 Leong-Škorničková et al. HB17 (paratype, SING: 0188968) Vietnam solitary verrucose verrucose no papillae
A. truongii BGMN 2013/2461W Rybkova et al. HB17 6484 (M: M0210863) Vietnam solitary verrucose verrucose no papillae
SBG Leong-Škorničková JLS1047 - Vietnam solitary verrucose verrucose no papillae
A. typica MBG 2017.12835.06 Tillich 5996 (M) Vietnam solitary smooth verrucose no papillae
A. vietnamensis BIN 786 Averyanov et al. HAL12116a (holotype, LE: LE01050347) Vietnam solitary verrucose verrucose no papillae
A. corniculata from nature Vislobokov 18089 (isotype, MW: MW0595715) Vietnam solitary rugose rugose no papillae V
A. erosa SBG Leong-Škorničková JLS2906 - Vietnam solitary verrucose rugose no papillae
A. foliosa BGMN 97/2360; Bogner 2502 Tillich 4471 (holotype, M: M0213541) Vietnam solitary rugose rugose no papillae
BGMN 97/2353 Bogner 2803 (M) Vietnam solitary rugose rugose no papillae
A. locii BGMN 96/3121; Arnautov 86-112 Tillich 4359 (M: MSB004976) Vietnam solitary verrucose rugose no papillae
BIN 86-169 Arnautov 86-112 (LE: LE01055472) Vietnam solitary verrucose rugose no papillae
A. lubae var. lancifolia BIN CPC1566 Averyanov et al. CPC1566 (holotype, LE: LE01050389) Vietnam solitary verrucose rugose no papillae
A. lubae var. lubae BIN 13266 Averyanov et al. CPC6962 (LE: LE01049991) Vietnam solitary verrucose rugose no papillae
A. multiflora MBG 2015.11375.01 Vislobokov 14045 (MW: MW0750152) Vietnam solitary rugose rugose no papillae
A. xuansonensis MBG 2015.11366.01 Vislobokov 13102 (paratype, MW: MW0591740) Vietnam solitary verrucose rugose no papillae
A. bicolor BGMN 97/2352; Bogner 2503 Tillich 4462 (holotype, M: M0213531) unknown solitary verrucose smooth low VI
A. fungilliformis MBG 2016.12350.02 Vislobokov et al. G63 (MW: MW0753782) China solitary smooth smooth low
MBG 2016.12355.01 Vislobokov et al. G82 (MW: MW0753780) China solitary smooth smooth low
A. geastrum BGMN 97/2375G Tillich 4598 (holotype, M: M0213544) Vietnam solitary smooth smooth low
A. longipetala MBG 2017.13459.01 Vislobokov et al. G111 (MW: MW0754777) China solitary smooth smooth low
A. papillata from nature Vislobokov 18087 (MW: MW0756241) Vietnam solitary smooth smooth low
A. tillichiana var. latifolia BIN 13270 Averyanov et al. CPC6841 (holotype, LE: LE01050358) Vietnam solitary smooth smooth low VI
A. clausa from nature Vislobokov 18090 (MW: MW0756227) Vietnam solitary verrucose verrucose low VII
A. connata BGMN 97/2358 Bogner 2495 (M) Vietnam solitary smooth verrucose low
A. opaca from nature Vislobokov 18035 (MW: MW0756235) Vietnam solitary verrucose verrucose low
A. semiaperta BIN 11614 Averyanov et al. CPC1566b (LE: isotype, LE01050394) Vietnam solitary smooth verrucose low
A. subrotata var. subrotata from nature Vislobokov et al. A.s.5 (MW: MW0735059) Thailand solitary verrucose verrucose low
A. subrotata var. angustifolia MBG 2015.11355.01 Vislobokov et al. A.s.1 (MW: MW0735069) Thailand solitary verrucose verrucose low
A. minor MBG 2018.14282.01 Nuraliev et al. 1966A (holotype, MW: MW0595716) Vietnam solitary rugose rugose low VIII
A. hekouensis BGMN 95/2832; Bogner 2216 Tillich 5005 (M: M0213547) China solitary smooth smooth medium IX
A. longanensis BIN 260301 - Vietnam solitary smooth smooth medium
A. lutea BGMN 96/3126; Arnautov 76-140 Tillich 4481 (holotype, M: M0213551) Vietnam solitary smooth smooth medium
BIN 17304 Tillich 5003 Arnautov 76-140 (paratype, LE: LE01049990) Vietnam solitary smooth smooth medium
A. sinensis BIN 13659 Arnautova s.n. (holotype, LE: LE01050480) China solitary smooth smooth medium
A. stricta BGMN 96/3124; Arnautov 88-110 Tillich 4367 (holotype, M: M0213560) Vietnam solitary smooth smooth medium
A. subrotata var. subrotata SBG 20121895; Leong-Skornickova JLS1558 - Vietnam solitary smooth smooth medium
A. superba BGMN 97/2369T; Bogner 2346 Tillich 4480 (paratype, M: M0213562) Vietnam solitary smooth smooth medium
A. arnautovii var. arnautovii BIN 18566 Averyanov AL466ED4 (LE: LE01048630) Vietnam solitary smooth verrucose medium X
BGMN 96/3123; Arnautov 88-115 Tillich 4474 (holotype, M: M0213528) Vietnam solitary smooth verrucose medium
MBG 2015.11353.01 Vislobokov 13042 (MW: MW0735025) Vietnam solitary smooth verrucose medium
A. arnautovii var. catbaensis BGMN 96/3125; Arnautov 88-144 Tillich 4460 (M: M0213526) Vietnam solitary verrucose verrucose medium
MBG 2015.11352.01 Vislobokov 13040 (MW: MW0735030) Vietnam solitary verrucose verrucose medium
A. connata BGMN 96/3119; Arnautov 85-722 Tillich 4470 (holotype, M: M0213538) Vietnam solitary smooth verrucose medium
BIN Arnautov 85-722 Tillich 5486 (paratype, LE: LE01050022) Vietnam solitary smooth verrucose medium
A. nutans BIN 13281 Averyanov et al. CPC7158b (holotype, LE: LE01032173) Vietnam solitary smooth verrucose medium
A. opaca var. opaca BGMN 2013/2460W; Rybkova et al. 180 - Vietnam solitary verrucose verrucose medium
BGMN 97/2359; Bogner 2491 Tillich 4468 (holotype, M: M0213554) Vietnam solitary verrucose verrucose medium
A. opaca var. opaca SBG 20111766 JLS1121 Vietnam solitary verrucose verrucose medium X
A. opaca var. rugosa BGMN 13/2460; Rybkova et al. 180 - Vietnam solitary verrucose verrucose medium
A. subrotata var. subrotata SBG Leong-Škorničková JLS2989 - Vietnam solitary smooth verrucose medium
A. subrotata var. subrotata BGMN 04/1769 - Vietnam solitary verrucose verrucose medium
A. zinaidae BIN 7242 Averyanov et al. HAL11111b (holotype, LE: LE01050435) Vietnam solitary rugose rugose medium XI
A. bogneri BIN 9311 - Vietnam solitary smooth smooth high XII
BGMN 97/2374W Bogner 2500 (paratype, M: M0213534) Vietnam solitary smooth smooth high
BGMN 97/2404 Bogner 2805 (paratype, M: M0213535) Vietnam solitary smooth smooth high
SBG 20120086; Leong-Škorničková JLS1436 - Vietnam solitary smooth smooth high
A. grandiflora BIN 11590 Harder et al. DKH 8123 (holotype, LE: LE01054814) Vietnam solitary smooth smooth high
A. letreae SBG Leong-Škorničková JLS2977 - Vietnam solitary smooth smooth high
A. magnifica MBG 2016.12423.01; Nuraliev 1672 Romanov et al. s.n. (MW) Vietnam solitary smooth smooth high
A. formosa SBG 20120060; Leong-Škorničková JLS1384 - Vietnam solitary verrucose verrucose high XIII
BGMN 1997/2367 Tillich 5280 (holotype, M: M0213543) unknown solitary verrucose verrucose high
SBG Leong-Škorničková JLS3178 - Vietnam solitary verrucose verrucose high
MBG 2015.11376.01 Vislobokov 14062 (MW: MW0750154) Vietnam solitary verrucose rugose high
BIN s.n. Averyanov et al. CPC6412 (LE: LE01050398) unknown solitary rugose rugose high
A. jiewhoei SBG Leong-Škorničková JLS1218 Vietnam solitary rugose rugose high
SBG 20122069 Leong-Skornickova JLS1871 (holotype, SING, isotype, M: M0225616) Vietnam solitary rugose rugose high
A. marasmioides BGMN 96/3118; Arnautov 88-117 Tillich 4458 (holotype, M: M0213552) Vietnam solitary rugose rugose high
MBG 2015.11354.01 Vislobokov 13046 (MW: MW0735052) Vietnam solitary rugose rugose high