Plant Inventory in the Solomon Islands, with Special Reference to Medicinal Plant Resources (4). Comparison of Dendrobium (Orchidaceae) Plant Components Using Multivariate Analysis

Koji Sugimura; Akihiro Daikonya; Hiroyuki Fuchino; Nobuyuki Tanaka; Fred Pitisopa; Takashi Watanabe

doi:10.1248/bpb.b24-00413

Abstract

Eight species of the genus Dendrobium were collected from the Solomon Islands. The morphological and compositional characteristics of their stems and leaves were studied and compared with two Japanese medicinal species of Dendrobium by using multivariate analysis of their components. As a result, we discovered that some types of Dendrobium plants from the Solomon Islands have a composition pattern comparable to that of the Japanese medicinal species, D. catenatum. Within the same species, distinct varieties with different compositions exist based on their locations in the Solomon Islands. Certain types also have different composition patterns depending on the stem and leaf sections. Our findings show that Dendrobium plants in the Solomon Islands have a distinct stem and leaf morphology and composition, while they also share similar compositional patterns with existing medicinal species. As a result, these plants are regarded as valuable medicinal resources with the potential to be used as novel crude drug ingredients.

INTRODUCTION

Over 20000 species of Orchidaceae are distributed worldwide, from the tropics to the cold regions.¹⁾ Dendrobium is the largest genus in the family, with approximately 1500 species found throughout Asia and Oceania, including the Pacific region.^1,2) Dendrobium plants thrive naturally in a wide variety of environments, including lowlands, mountains, and dry to humid areas.¹⁾ There are approximately 230 species of Orchidaceae in Japan, of which three belong to the genus Dendrobium that occur from Honshu to Ryukyu.³⁾ On the contrary, the Solomon Islands have one of the largest remaining tropical rain forests in the South Pacific,^4,5) as well as a diverse range of approximately 300 orchid species.⁶⁾ In addition, 55 species of Dendrobium are distributed in the Solomon Islands, with a significant diversity.^6,7)

Dendrobium stem (石斛, Sekkoku) is an important herbal medicine with a wide variety of functions, including stomachic, antipyretic, anti-inflammatory, and tonic actions.^8,9) Tonics have been used throughout Asia for over a millennium.¹⁰⁾ In particular, D. officinale Kimura & Migo and D. nobile Lindl. have excellent tonic properties.^11,12) In Japan, D. moniliforme (L.) Sw. and D. catenatum Lindl. are used in stomach and tonic medicines.^13–15) Dendrobium plant research focuses on its antioxidant,^16–18) blood sugar-lowering,^19,20) immunity-boosting,^21,22) tumor suppression,^23,24) as well as alkaloid^25–28) and phenolic components.^29,30) Dendrobium has been the subject of numerous component studies throughout Asia. Although Dendrobium plants from the South Pacific region, particularly the Solomon Islands, offer valuable study materials as underused plant resources, no investigations on their composition have been carried out.⁷⁾

This study of the morphological and compositional characteristics of Dendrobium stems and leaves was undertaken as part of the Plant Inventory in the Solomon Islands, with a focus on medicinal plant resources.^31–34) Furthermore, we used multivariate analysis to compare the components of Dendrobium plants grown in the Solomon Islands with plants of the same genus grown by the Tanegashima Research Department.

MATERIALS AND METHODS

Plant Material

The resource exploration survey was conducted on seven islands in the Solomon Islands (Fig. 1) and 12 species of Dendrobium were collected. Collection location and collection date, and substrate are shown in Table 1, along with the sample ID number. Details of sample identification are given in “Results”. The stems and leaves of D. mobile and D. catenatum used for comparison were prepared from samples grown in the greenhouse of the Tanegashima Research Department. The plant specimens are deposited at the herbarium of Kochi Prefectural Makino Botanical Garden (MBK), and the analytical samples are kept at the Research Center for Medicinal Plant Resources, National Institutes of Biomedical Innovation, Health and Nutrition.

Fig. 1. Collection Location in the Solomon Islands

Table 1. Dendrobium Plants (Orchidaceae) Used during Component Analysis

Sample ID	Species	Location	Epiphytic substrate	Collection date
SIMB 940*	Dendrobium erosum (Blume) Lindl.	Tetepare Island	Trunk	Jul. 30, 2009
SIMB 941*	Dendrobium rechingerorum Schltr.	Tetepare Island	Trunk	Jul. 30, 2009
SIMB 954*	Dendrobium mohlianum Rchb.f.	Tetepare Island	Trunk	Jul. 31, 2009
SIMB 967*	Dendrobium goldfinchii F.Muell.	Tetepare Island	Trunk	Aug. 1, 2009
SIMB 978*	Dendrobium salomonense Schltr.	Tetepare Island	Trunk	Aug. 1, 2009
SIMB 986*	Dendrobium rechingerorum Schltr.	Tetepare Island	Trunk	Aug. 1, 2009
SIMB 1062*	Dendrobium gouldii Rchb.f.	Sulei Island	Trunk	Aug. 10, 2009
SIMB 1100*	Dendrobium angustipetalum J.J.Sm.	Santa Isabel Island	Trunk	Aug. 12, 2009
SIMB 152*	Dendrobium comatum (Blume) Lindl.	New Georgia Island	Trunk	Aug. 4, 2008
SIMB 1681*	Dendrobium gouldii Rchb.f.	San Cristobal Island	Trunk	Sep. 5, 2011
SIMB 1829*	Dendrobium gouldii Rchb.f.	Three Sisters Islands	Trunk	Sep. 9, 2011
SIMB 1942*	Dendrobium gouldii Rchb.f.	Pio Island	Trunk	Sep. 2, 2011
M 76**	Dendrobium nobile Lindl.	Tanegashima Island	Trunk	Mar. 2, 2011
R 66**	Dendrobium catenatum Lindl.	Tanegashima Island	Trunk	Mar. 2, 2011

*Wild plants from the Solomon Islands. **Cultivated plants from Japan.

Morphological Investigation of Leaf and Stem

The morphology of the stems was examined, and the shape, length, branching, presence or absence of nodes, and vertical striations were recorded. Leaf morphology was observed, and leaf shape, length, width, and petioles were measured. The shapes were sorted into two types: upright and hanging. The growth forms were classified into two types: upright and drooping. Stem length was classified into four categories: short (<10 cm), medium (≥10 cm but <30 cm), long (≥30 cm but <50 cm), and exceptionally long (≥50). The branches were divided into two categories: not applicable (N) and applicable (A). The nodes were divided into two categories: not applicable (N) and applicable (A). The vertical stripes of the stems were classified into two types: clear and unclear. The leaf shape was divided into five types: lanceolate, linear, falcate, oblong, and elliptical. Leaf length was classified into three categories: short (<5 cm and <10 cm), medium (10 cm to <15 cm), and long (≥15 cm). Leaf width was divided into three categories: narrow (<1.5 cm), medium (≥1.5 cm but <3 cm), and wide (≥3 cm). Petioles were classified into two categories: not applicable (N) and applicable (A).

Preparation of Stems and Leaves

The stems and leaves were separated and shredded, then dried for 3 d in the shade and for 48 h in a dryer (EPFH-343-2T; Isuzu, Yokohama, Japan) using warm air at 50°C.

Component Analysis of Stems and Leaves

Plants of the genus Dendrobium collected from the Solomon Islands, as well as the stems and leaves of plants grown at the Seed Research Department, were evaluated using LC/MS to determine the presence of various compounds.

We weighed 0.5 g each of the powdered dried stems and leaves, added 20 mL of 80% methanol, and ultrasonically extracted the mixtures for 45 min. The extracts were analyzed using liquid chromatography and mass spectrometry. The Agilent 1100 series chromatograph (Agilent Technologies Inc., Santa Clara, CA, U.S.A.) was used under the following conditions: column: Xbridge (150 × 4.6 mm, 5 µm) (Waters Corp., Milford, MA, U.S.A.); column temperature: 40°C; flow rate: 0.5 mL/min. The mobile phases were A) 0.1% acetic acid/H₂O and B) 0.1% acetic acid/CH₃CN. 10% B at 0 min; linear gradient to 40% B at 30 min; 80% at 45 min and then hold at 80 min. The sample injection volume was 1 µL. The conditions for the mass spectrometer (API 3000; AB Sciex LLC., Framingham, MA, U.S.A.) were as follows: Ionization method: APCI; Intake mass: m/z 100–1000; NED: 10; CUR: 10; NC: 2; and desolvation temperature: 400°C.

Principal Component Analysis

Principal component analysis (PCA) was used to classify the different stem and leaf components and the geographical origin of Dendrobium plant samples. For this purpose, we used LC/MS data of Dendrobium plants. LC/MS data were alignment using SIEVE (Thermo Fisher Scientific, Waltham, MA, U.S.A.), and peak picking was performed using MassLynx (Waters, Milford, MA, U.S.A.). MarkerView software (AB Sciex LLC., Framingham, MA, U.S.A.), a multivariate analysis software, was used to analyze the matrix data. Pareto scaling was selected as data scaling.

RESULTS

Identification and Morphological Comparison of Dendrobium Plants

Eight species were identified based on the morphological observations of the flowers, stems, and leaves of voucher specimens and a literature search^6,7,35,36) (Table 1). Further identification was carried out by comparing with specimens stored at the Solomon Islands National Herbarium (BSIP) in Honiara. Photographs of each species are shown in Fig. 2. Table 2 shows the morphological characteristics of the stems and leaves of 10 species of Dendrobium plants, including 8 wild species from the Solomon Islands and 2 cultivated medicinal species in Japan.

Fig. 2. Photos of the Dendrobium Plant Growth Types

Table 2. Morphological Characteristics of the Stems and Leaves of 10 Species of Dendrobium Plants

Species	Stem characteristics					Leaf characteristics
Species	Growth form	Stem length *	Branching N/A	Nude N/A	Vertical stripes of stem	Leaf shape	Leaf length **	Leaf width ***	Petiole N/A
D. angustipetalum	Upright	Short	N	A	Clear	Linear	Short	Narrow	N
D. nobile	Upright	Medium	N	A	Unclear	Oblong	Medium	Wide	N
D. goldfinchii	Upright	Medium	N	A	Unclear	Falcate	Short	Narrow	N
D. gouldii	Upright	Long	N	A	Clear	Lanceolate	Long	Medium	N
D. rechingerorum	Upright	Long	N	A	Unclear	Oblong	Medium	Medium	N
D. comatum	Upright	Long	A	A	Clear	Elliptic	Medium	Wide	N
D. catenatum	Drooping	Medium	N	A	Clear	Linear	Short	Wide	N
D. mohlianum	Drooping	Especially long	N	A	Unclear	Lanceolate	Long	Medium	N
D. erosum	Drooping	Especially long	N	A	Unclear	Linear	Medium	Medium	N
D. salomonense	Drooping	Especially long	N	A	Unclear	Linear	Medium	Narrow	N

*Stem length; Short (<10 cm), Medium (≥10 cm and <30 cm), Long (≥30 cm and <50 cm), Especially long (≥50 cm). **Leaf length; Short (<10 cm), Medium (≥10 cm and <15 cm), Long (≥15 cm). ***Leaf width; Narrow (<1.5 cm), Medium (≥1.5 cm and <3 cm), Wide (≥3 cm).

Dendrobium plants from the Solomon Islands have significantly larger stems than those grown in Japan. We also found species with particularly long stems. Many species are unbranched, with nodes, and indistinct vertical veins on their stems. Furthermore, leaf lengths and widths varied, and all species lacked petioles and grew on tree trunks. Specifically, D. angustipetalum J.J.Sm. had the shortest stems and the smallest leaves of the Solomon Islands species, as well as characteristics similar to those of D. moniliforme, which grows in Japan. Dendrobium goldfinchii F.Muell. has unusually fleshy and sword-shaped leaves, whereas D. rechingerorum has relatively round and short leaves compared with the other species. Dendrobium comatum (Blume) Lindl. has stem and leaf characteristics similar to other Dendrobium species, although previously classified in a different genus Flickingeria.³⁷⁾ The results of the present compositional analysis also support the affiliation of this species to Dendrobium.

Comparison of the Components of Dendrobium Plants

LC/MS analysis was performed, and the obtained data were applied to PCA analysis to evaluate the diversity of the component composition and to compare it with Japanese medicinal species. Figures 3 and 4 show the PCA results (APCl-Neg) for Dendrobium plant stems and leaves, respectively, obtained using MarkerView software.

Fig. 3. PCA Results (APCl-Neg) for Stems of Dendrobium Plants Using MarkerView

1: Dendrobium salomonense (SIMB 978), D. angustipetalum (SIMB 1100). 2: D. gouldii (SIMB 1681). 3: D. gouldii (SIMB 1829, SIMB 1942). 4: D. catenatum (R 66), D. erosum (SIMB 940), D. goldfinchii (SIMB 967), D. gouldii (SIMB 1062), D. mohlianum (SIMB 954), D. rechingerorum (SIMB 941, SIMB 986), D. comatum (SIMB 152). 5: D. nobile (M 76). Numbers in parentheses are sample ID.

Fig. 4. PCA Results (APCl-Neg) for Leaves of Dendrobium Plants Using MarkerView

1: Dendrobium salomonense (SIMB 978), D. angustipetalum (SIMB 1100). 2: D. comatum (SIMB 152). 3: D. catenatum (R 66), D. nobile (M 76), D. erosum (SIMB 940), D. goldfinchii (SIMB 967), D. gouldii (SIMB 1062, 1681, 1829, 1942), D. mohlianum (SIMB 954), D. rechingerorum (SIMB 941), D. rechingerorum (SIMB 986). The numbers in parentheses are sample ID.

The results of PCA analysis of the analytical data of the stems and leaves are shown in Figs. 3 and 4, respectively. In Fig. 3, the cumulative contribution rate up to the second component for the stem was 43.2% (25.3% for PC1 and 17.9% for PC2). In Fig. 4, the cumulative contribution rate up to the second component for the leaf was 83.6% (53.3% for PC1 and 30.3% for PC2). PCA revealed that stems could be classified into five groups and leaves into three groups. The representative chromatograms corresponding to the five groups found in the stems are shown in Fig. 5.

Fig. 5. HPLC Total Ion Chromatograms (TIC, APCI-Neg) of 14 Samples of Dendrobium Stems

PCA in multivariate analysis revealed that stems could be classified into five groups and leaves into three. The stems of Dendrobium from Solomon Islands, specifically stem group 1 (D. salomonense: SIMB 978, D. angustipetalum: SIMB 1100) had high scores and loadings of PC2, and stem group 2 (D. gouldii: SIMB 1681) had high scores and loadings of PC1 and PC2, which were different from the other samples. Therefore, these samples may contain characteristic components. D. gouldii collected in the Solomon Islands was found growing on the Three Sisters Islands (SIMB 1829) and Pio Island (SIMB 1942), and was classified into the same stem group 3, suggesting similarity in the components contained therein. D. catenatum (R 66) cultivated in Japan and D. erasum (SIMB 940), D. goldfinchii (SIMB 967), D. gouldii (SIMB 1062), D. mohlianum (SIMB 954), D. rechingerorum (SIMB 941), and D. rechingerorum (SIMB 986) collected in the Solomon Islands were classified in the same stem group 4, suggesting similarity in the components contained. D. nobile (M 76) cultivated in Japan and D. comatum (SIMB 152) collected in the Solomon Islands were classified in the same stem group 5, suggesting similarity in the components contained. In addition, leaf group 1 (D. salomonense: SIMB 978, D. angustipetalum: SIMB 1100) had a high score and loading value for PC2, and leaf group 2 (D. comatum: SIMB 152) had a high score and loading value for PC1, which were different from the other samples. Therefore, these samples may contain characteristic components.

The above data indicate that some Dendrobium plants collected in the Solomon Islands have compositional patterns that are similar to the Japanese medicinal species D. catenatum and D. nobile and may serve as substitutes.

As indicated by the wavy line frames, peaks characteristic of each species were observed, such as D. goldfinchii (SIMB 967) and D. rechingerorum (SIMB 941, 986) in stem group 4, and D. comatum (SIMB 152) in stem group 5. Further investigation is required to evaluate these peaks, for example, by increasing the number of samples.

DISCUSSION

The genus Dendrobium is extremely diverse and hasr been used as medicinal plants since antiquity.^8,11) However, the plants that are actually used medicinally are limited to a small number of species spread throughout Asia.⁹⁾ Dendrobium officinale and D. nobile are the most commonly used; many ingredient studies have been conducted, and the effectiveness of these species has been extensively studied.^38–41) Recent studies have examined Alzheimer’s disease,⁴²⁾ anti-aging,⁴³⁾ and photoaging protection.⁴⁴⁾ As previously stated, Dendrobium plants continue to garner attention as a resource for drug discovery. Although the Solomon Islands in the South Pacific region are the global distribution center for the Dendrobium species, with extremely high species diversity, little research has been undertaken on the compositional characteristics of each species.

As a result, this study defined the morphology and composition of Dendrobium plants found in the Solomon Islands. Furthermore, we used multivariate analysis to compare the components of plants in the genus Dendrobium, examining differences in components by dividing them into stems and leaves, as well as by species or by region. Although the scores varied, the first principal component tended to separate the species into groups that were chemically close to D. gouldii and groups that were chemically distant from it. The second principal component also tended to separate the medicinal species D. nobile and D. catenatum into groups that were chemically close to it and groups that were chemically distant from it.

These results enabled us to classify the stem groups of the Solomon Islands Dendrobium plants that have components similar to those of medicinal species. Among the Dendrobium plants collected in the Solomon Islands, five species (D. erosum, D. goldfinchii, D. gouldii, D. mohlianum, D. rechingerorum) have chemical patterns similar to those of the Japanese medicinal species D. catenatum (R 66), and are expected to be useful. Therefore, species with similar chemical patterns as those currently used for medicinal purposes may be substitutes, and leaves with chemical patterns different from those of traditionally used stems may contribute to the effective use of unused chemicals. These results indicate that Dendrobium plants collected in the Solomon Islands exhibit more diverse traits than those grown in Japan. Moreover, our monitoring survey of traditional doctors in the Solomon Islands confirmed that some Dendrobium plant species are used during fever.³²⁾

Based on the above, Dendrobium plants collected from the Solomon Islands are considered an extremely valuable plant group with great potential as a new medicinal plant resource. To effectively use the wide variety of Dendrobium plants obtained from the Solomon Islands in the future, it is important to study the characteristics of each species in-depth.

Acknowledgments

The authors acknowledge the support of the Tanegashima Experiment Station, Research Center for Medicinal Plant Resources, Japan, for the cultivation management during the study. They also express their sincere gratitude to the late Mr. Tofu Patterson of the Ministry of Forestry, National Herbarium and Botanical Garden Division for his cooperation in the botanical survey in the Solomon Islands.

Funding

This research was part of a joint research project supported by the Ministry of Education, Culture, Sports, Science, and Technology’s Grant-in-Aid for Scientific Research (A) Overseas Academic Research, Project No.: 20256003.

Author Contributions

K.S. and H.F. designed the study. K.S., T.W., N.T., and F.P. collected and authenticated the Dendrobium plants from Solomon Islands. K.S. cultivated Dendrobium plants at the Tanegashima Experiment Station. A.D. and H.F. performed the experiments. A.D. performed the multivariate, LC/MS analyses. T.W. supervision. K.S. wrote the manuscript. All the authors have read and approved the final version of the manuscript.

Conflict of Interest

The authors declare no conflict of interest.

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