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. 2017 May 25;22(6):879. doi: 10.3390/molecules22060879

Floral Scent Chemistry of Luculia yunnanensis (Rubiaceae), a Species Endemic to China with Sweetly Fragrant Flowers

Yuying Li 1, Youming Wan 1, Zhenghai Sun 2, Taiqiang Li 1, Xiongfang Liu 1, Hong Ma 1,*, Xiuxian Liu 1, Rui He 1, Yan Ma 1, Zhenghong Li 1,*
Editor: Derek J McPhee
PMCID: PMC6152718  PMID: 28587077

Abstract

Luculia plants are famed ornamentals with sweetly fragrant flowers. Luculia yunnanensis Hu is an endemic plant from Yunnan Province, China. Headspace-solid phase microextraction-gas chromatography-mass spectrometry (HS-SPME-GC-MS) was used to identify the volatile organic compounds (VOCs) of the different flower development stages of L. yunnanensis for the evaluation of floral volatile polymorphism. The results showed that a total of 40 compounds were identified at four different stages. The main aroma-active compounds were 3-carene, α-cubebene, α-copaene, δ-cadinene, and isoledene. Floral scent emission had the tendency to ascend first and descend in succession, reaching its peak level at the initial-flowering stage. The richest diversity of floral volatiles was detected at the full-flowering stage. Principal component analysis (PCA) indicated that the composition and its relative content of floral scent differed at the whole flower development stage. In comparison with the other two species of Luculia (L. pinceana and L. gratissima), the composition and its relative content of floral scent were also different among the tree species.

Keywords: Luculia, volatile organic compound, SPME-GC-MS, floral scent, flower development

1. Introduction

The genus of Luculia Sweet comprises small trees or shrubs belonging to the Rubiaceae family (Trib. Cinchoneae). It has about five species in the world, mainly distributed in Southeastern Asia. There are three species distributed in China; i.e., L. pinceana Hooker, L. gratissima (Wallich) Sweet and L. yunnanensis Hu. Among them, L. yunnanensis is the unique one, endemic to Yunnan Province and naturally confined to open slopes and secondary shrubby woodland on limestone mountains at an altitude between 1200 and 3200 m [1]. Luculia species can be easily recognized by the compact and long-term blooming inflorescences consisting of white, pink to red, and sweetly fragrant flowers with extremely long corolla tubes [2]. L. yunnanensis distinguishes itself from its allied species by the surface of inflorescence axes, the hypanthium portion of the calyx, and its fruit covered by densely tomentose pubescences. Moreover, it is difficult to find wild populations of L. yunnanensis, as its appropriate habitats have been fragmented by human activities [1,3].

Plants synthesize a wide variety of volatile organic compounds (VOCs) that facilitate interactions with their lived environment: attracting pollinators, protecting flowers from harmful insects, and communicating with other plants. The floral scent compositions of L. pinceana and L. gratissima have been reported [4,5]. The main components of floral scent are paeonol and γ-murolene in L. pinceana and L. gratissima, respectively. Therefore, detecting the VOCs of L. yunnanensis could not only give clues to its conservation biology, but also provide reference to the development of L. yunnanensis as an ornamental with fragrant scent in the future.

Though the species of family Rubiaceae are not common aromatic plants, Luculia plants have a promising prospect as an essential oil source. Components and proportions of VOCs may vary at different flower developmental stages. Therefore, it is essential to investigate the VOCs polymorphism of different stages of flower development for determination of the suitable period for L. yunnanensis flower harvest.

Headspace solid phase micro-extraction (HS-SPME) followed by capillary gas-chromatography mass-spectrometry (GC-MS) has high reproducibility under the same test conditions, and is currently a widely used technique for flower volatile analysis [6,7]. In this paper, we investigated the floral volatiles in L. yunnanensis using HS-SPME coupled with GC-MS to evaluate the volatile polymorphism of different flower development stages, which provide guidance for the evaluation of flower scent quality and the generation of fragrant L. yunnanensis for future breeding programs and the function of floral fragrance.

2. Results and Discussion

2.1. Identification of Scent Components

The volatiles of four different stages of L. yunnanensis flower development (Figure 1) are given in Table 1, with the compounds listed in order of their retention time (RT) in the DB-5MS column. A total of forty VOCs were detected in L. yunnanensis flower development. Among these volatiles, 22 compounds were identified in four different stages. The main aroma-active compounds were identified at 3-carene, α-cubebene, α-copaene, δ-cadinene, and isoledene; these compounds might dominate the fragrance of L. yunnanensis. For instance, 3-carene smells like lemon or resin, α-cubebene smells like herb or wax, α-copaene smells like wood or spice, δ-cadinene smells like thyme and medicine or wood [8]. Together, the volatile compounds form the delightful fragrance of the L. yunnanensis flower.

Figure 1.

Figure 1

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Different development stages of L. yunnanensis and its habitat. (I) bud stage; (II) initial-flowering stage; (III) full-flowering stage; (IV) end-flower stage; (V) habitat of L. yunnanensis.

Table 1.

Volatile compounds identified in four different stages of L. yunnanensis flower development using headspace solid phase micro-extraction (HS-SPME) coupled with gas-chromatography mass-spectrometry (GC-MS) (HS-SPME-GC-MS). (I) bud stage; (II) initial-flowering stage; (III) full-flowering stage; and (IV) end-flower stage.

Peak RT LRI LRI * Compounds CAS # Relative Content (%) ± SD
I II III IV
Monoterpenes
1 8.35 903 929 (1S)-2,6,6-Trimethylbicyclo[3.1.1]hept-2-ene 7785-26-4 0b 0b 0.25 ± 0.06a 00b
2 8.72 916 910 Santolina triene 2153-66-4 0b 0.01 ± 0.01b 0.16 ± 0.08a 00b
3 9.45 943 941 -α-Pinene 80-56-8 0b 0b 0.99 ± 0.20a 00b
4 9.81 957 966 β-Pinene 127-91-3 0b 0.09 ± 0.01b 0.07 ± 0.04b 0.42 ± 0.10a
7 11.32 1011 1011 3-Carene 13466-78-9 3.36 ± 0.44c 10.72 ± 2.20b 9.17 ± 1.65bc 29.18 ± 4.53a
8 12.63 1059 1056 trans-β-Ocimene 3779-61-1 0.88 ± 0.10b 0.61 ± 0.13b 0.99 ± 0.49b 1.86 ± 0.04a
11 13.81 1102 1127 α-Campholenal 91819-58-8 0b 0b 0.60 ± 0.30a 00b
12 14.37 1124 - α-Santoline alcohol 90823-36-2 0b 0b 0.35 ± 0.18a 0b
13 14.84 1142 1137 Limonene oxide 1195-92-2 0.20 ± 0.14a 0a 0.28 ± 0.19a 0a
Aliphatics
5 10.64 987 987 Methyl heptenone 110-93-0 0.68 ± 0.26a 0b 0b 0b
6 11.14 1005 - Furan, 2,3-dihydro-4-(1-methylethyl)- 34314-84-6 3.27 ± 0.89a 0.33 ± 0.02b 0.17 ± 0.03b 1.07 ± 0.05b
9 13.46 1089 1130 2,6-Dimethyl-1,3,5,7-octatetraene 460-01-5 0b 0b 0.29 ± 0.08a 0b
15 19.67 1340 1373 Propanoic acid, 2-methyl-, 2-ethyl-3-hydroxyhexyl ester 74367-31-0 1.12 ± 0.13a 0.25 ± 0.05b 0.22 ± 0.11b 1.16 ± 0.14a
40 28.08 1828 1827 Isopropyl myristate 110-27-0 0b 0b 0.18 ± 0.06b 1.51 ± 0.15a
Benzenoids
10 13.71 1098 1107 Phenylethyl alcohol 60-12-8 0b 0.10 ± 0.02a 0b 0b
14 18.31 1295 - 6,7-Dimethyl-1,2,3,5,8,8a -hexahydronaphthalene 107914-92-1 0b 0.14 ± 0.03a 0.17 ± 0.09a 0b
22 22.45 1433 1451 Paeonol 552-41-0 0b 0b 12.73 ± 2.43a 0b
36 24.99 1550 1550 Benzene, 1,2,3-trimethoxy-5-(2-propenyl)- 487-11-6 0c 0.41 ± 0.03a 0c 0.13 ± 0.07b
Sesquiterpenes
16 19.87 1346 1346 α-Cubebene 17699-14-8 13.39 ± 0.63a 10.24 ± 1.68b 8.68 ± 1.09b 7.52 ± 1.02b
17 20.34 1361 1365 α-Copaene 3856-25-5 16.59 ± 3.43a 17.92 ± 2.73a 9.30 ± 0.73b 7.45 ± 0.49b
18 21.13 1387 1377 Isoledene 95910-36-4 9.79 ± 1.21a 8.67 ± 0.65a 8.33 ± 1.94a 7.19 ± 1.40a
19 21.52 1399 1400 Caryophyllene 87-44-5 4.23 ± 0.49a 2.05 ± 0.12b 1.19 ± 0.26b 3.76 ± 0.69a
20 21.87 1412 1421 β-Ylangene 20479-06-5 0.60 ± 0.01a 0.34 ± 0.07b 0.08 ± 0.03c 0.36 ± 0.02b
21 22.22 1425 1438 α-Guaiene 3691-12-1 0b 0.12 ± 0.03a 0.04 ± 0.02b 0b
23 22.68 1441 1450 cis-Muurola-3,5-diene Not available 3.43 ± 0.36ab 3.76 ± 0.50ab 4.48 ± 1.17a 2.61 ± 0.48b
24 22.81 1447 1446 Humulene 6753-98-6 3.89 ± 0.68b 1.70 ± 0.21c 3.42 ± 1.29bc 9.69 ± 0.49a
25 23.01 1454 1458 β-Gurjunene 17334-55-3 0b 0.23 ± 0.07a 0.04 ± 0.02a 0b
26 23.32 1466 1474 β-Cadinene 523-47-7 2.27 ± 0.06a 1.63 ± 0.20a 2.42 ± 0.64a 1.61 ± 0.55a
27 23.42 1469 1475 Naphthalene,1,2,4a,5,6,8a -hexahydro-4,7-dimethyl-1-(1-methylethyl)- 483-75-0 0b 0.66 ± 0.08a 0.08 ± 0.05b 0.77 ± 0.01a
28 23.56 1474 1474 γ-Muurolene 30021-74-0 3.15 ± 0.33b 4.50 ± 0.77a 1.79 ± 0.48c 1.95 ± 0.22bc
29 23.84 1485 1515 Cubebol 23445-02-5 4.36 ± 0.42a 3.89 ± 0.64a 3.85 ± 0.41a 2.52 ± 0.41b
30 23.97 1490 1484 -Aristolene 6831-16-9 1.05 ± 0.14a 0.83 ± 0.06ab 1.01 ± 0.41a 0.42 ± 0.02b
31 24.07 1493 1500 (E,E)-α-Farnesene 502-61-4 0.42 ± 0.02b 1.36 ± 0.26b 4.65 ± 1.13a 1.21 ± 0.07b
32 24.29 1503 1494 4-epi-Cubebol Not available 4.24 ± 0.51b 9.06 ± 1.41a 4.67 ± 1.48b 2.90 ± 0.73b
33 24.44 1514 1519 δ-Cadinene 483-76-1 14.66 ± 2.85a 12.68 ± 2.56a 13.07 ± 2.79a 9.16 ± 0.77a
34 24.62 1525 1528 Cadine-1,4-diene 16728-99-7 5.74 ± 0.05ab 6.13 ± 0.73a 4.47 ± 1.86ab 3.13 ± 0.25b
35 24.87 1542 1542 α-Calacorene 21391-99-1 0c 0.32 ± 0.06a 0.18 ± 0.04b 0c
37 25.68 1596 1596 Guaiol 489-86-1 1.09 ± 0.14a 0.24 ± 0.07b 0.30 ± 0.04b 1.11 ± 0.27a
38 25.82 1608 1630 α-Acorenol 28296-85-7 0.72 ± 0.09a 0.30 ± 0.04b 0.33 ± 0.05b 0.73 ± 0.15a
39 26.32 1652 1647 Cubenol 21284-22-0 0.81 ± 0.01a 0.71 ± 0.02a 1.00 ± 0.43a 0.58 ± 0.01a
Monoterpenes 4.50 ± 0.41c (9.11%) 11.43 ± 2.31bc (20.21%) 12.86 ± 2.93b (22.78%) 31.46 ± 4.46a (14.18%)
Aliphatics 5.07 ± 0.75a (14.79%) 0.58 ± 0.08c (13.79%) 0.86 ± 0.25c (29.07%) 3.74 ± 0.33b (8.82%)
Benzenoids 0b 0.65 ± 0.07b (10.77%) 12.90 ± 2.35a (18.22%) 0.13 ± 0.07b (53.85%)
Sesquiterpenes 90.43 ± 1.17a (1.29%) 87.34 ± 2.46a (2.82%) 73.38 ± 5.20b (7.09%) 64.67 ± 4.09b (6.32%)
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Values, expressed as mean ± SD of triplicate measurements, with different letter (a–c) in the same row indicating significant difference according to Tukey’s test (p < 0.05). The data in brackets are coefficients of variation. RT: retention time; LRI: linear retention index; LRI *: linear rentention index taken from NIST Standard Reference Database 69 [15]; CAS #: chemical abstracts service registry number.

As we all know, floral scent often serves as an olfactory signal for the attraction of insects. For example, bees can find the location of flowers under the guidance of linalool or 2-phenylethanol [9]; and indole for flies [10]; phenylacetaldehyde, 2-phenylethanol, oxoisophorone, linalool, and linalool oxide for butterflies [11], etc. Most visitors successfully transfer the pollen to conspecific flowers as pollinators [12]. To survive biotic stresses, many plant species have developed elaborate mechanisms to protect themselves against insects (e.g., emitting floral VOCs). (E,E)-α-Farnesene emitted from the flowers of Prorhinotermes canalifrons functioned as an alarm pheromone [13]. Besides (E,E)-α-farnesene, trans-β-ocimene (which can elicit strong antennal responses in butterfly [14]) also appeared in L. yunnanensis. Our preliminary results showed that the visiting insects of L. yunnanensis flowers in the field included Apis florae, Bombus sp., Lucillia sp., etc. (Figure 2).

Figure 2.

Figure 2

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Flowers of L. yunnanensis visited by different insects.

In addition, some compounds of floral VOCs had a good effect on resisting bacteria and fungus [7,16,17]. Amongst the floral scent composition of L. yunnanensis, phenylethyl alcohol has antifungal activity against Botrytis cinerea [18]; limonene oxide has antibacterial activities against Agrobacterium tumefaciens, Erwinia ananas, Erwinia chrysanthemi, and Enterobacter cloacae [19]; paeonol has potential acaricide activity for the control of Dermatophagoides pteronyssinus and Dermatophagoides farina [16]. From this point of view, L. yunnanensis might be qualified as an indoor fragrant houseplant. Recent studies have shown that plants can rapidly alter their own floral volatile production in response to floral volatile cues from their neighbors in flower opening [20,21]. This specific mechanism can increase the rate of pollination and mating by increasing floral volatile emission to attract more pollinators. The relationship between the floral VOCs of L. yunnanensis and its environment needs further research in the future.

2.2. Changes of Scent Emission in Four Different Stages

L. yunnanensis flowers were selected on the basis of their botanical characteristics to evaluate floral volatile polymorphisms according to different development stages: bud stage, initial-flowering stage, full-flowering stage, and end-flowering stage. The floral scents are orchestrated during the flower development. Table 1 and Figure 3 show the distinct changes in scent composition and concentration across flowering stages. Scent components were emitted drastically at the initial-flowering stage. The highest diversity of floral volatiles was detected at the full-flowering stage. In most plants (e.g., citrus flowers [22], Vanda Mimi Palmer [23], Cananga odorata [24], Ocimum citriodorum [25], Penstemon digitalis [26], and Hosta flowers [27]), the amount of scent emission and the diversity of floral volatiles were sharply increased at the stage of full bloom and decreased highly after full bloom. By contrast, the patterns of scent emission across L. yunnanensis flowering stages are different from one other.

Figure 3.

Figure 3

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Total ionic chromatogram of scent components emitted from the flowers of L. yunnanensis in different stages. (I) bud stage; (II) initial-flowering stage; (III) full-flowering stage; and (IV) end-flower stage.

As for the bud stage, 24 volatile compounds were identified, and the most abundant compounds were α-copaene (16.59%), δ-cadinene (14.66%), α-cubebene (13.39%), and isoledene (9.79%). For the initial-flowering stage, 31 volatile compounds were identified, and the most abundant compounds were α-copaene (17.92%), δ-cadinene (12.68%), 3-carene (10.72%), and α-cubebene (10.24%). For the full-flowering stage, 37 volatile compounds were identified, and the most abundant compounds were δ-cadinene (13.07%), paeonol (12.73%), α-copaene (9.30%), and 3-carene (9.17%). In the end-flowering stage, 26 volatile compounds were identified, and the abundant compounds were 3-carene (29.18%), humulene (9.69%), and δ-cadinene (9.16%).

The mean Bray–Curtis similarity index range was 64.29–81.40% (Table 2). The bud stage was more similar to the initial-flowering stage (BCS = 81.40%) than to the full-flowering stage (BCS = 71.88%), and was largely dissimilar to the end-flowering stage (BCS = 63.71%). Across all flower-life stages, the end-flowering stage was largely dissimilar to other three stages. Regarding the comparison among the studied stages, 22 volatiles among the total volatile constituents notably existed in all life-flower stages. The results showed high similarity among the four stages, although several constitutes (α-pinene, α-campholenal, phenylethyl alcohol, paeonol, etc.) were exclusively identified in different stages.

Table 2.

The Bray–Curtis similarity values (%) among stages of flower development of L. yunnanensis. (I) bud stage; (II) initial-flowering stage; (III) full-flowering stage; and (IV) end-flower stage.

I II III IV
I 100
II 81.40 100
III 71.88 76.30 100
IV 63.71 65.67 64.29 100
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To identify which volatiles contributed the most to the differences among the four flower stages, the data on 40 volatile compounds identified in L. yunnanensis at whole life-flower scale were analyzed by using principal component analysis (PCA). The first two components of PCA explained 36.61% and 29.36% of the variation, explaining ~66% of combined variance (Figure 4). The volatiles that had high positive scores on PC 1 included propanoic acid, 2-methyl-, 2-ethyl-3-hydroxyhexyl ester, caryophyllene, α-acorenol, guaiol, and β-ylangene, which were highly positively related to the bud stage and the initial-flowering stage. Volatiles with high positive scores on PC 2 comprised trans-β-ocimene, humulene, isopropyl myristate, α-campholenal, and α-santoline alcohol, which were positively correlated with the full-flowering stage and initial-flowering stage.

Figure 4.

Figure 4

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Principal component plot (PC1 vs. PC2 plots) for L. yunnanensis at different stages of growth, showing correlations with volatiles (numbers correspond to those in Table 1). (I) bud stage; (II) initial-flowering stage; (III) full-flowering stage; (IV) end-flower stage.

2.3. Variation in Volatile Compounds from Three Species of Luculia

Sesquiterpenes were the most abundant amongst floral scent compounds, the content of which reached as high as 64% in L. yunnanensis and L. gratissima [5], in the floral scent of L. pinceana were benzenoids [4]. By PCA analysis, the floral scent showed differences among Luculia (the wide-open flower of L. gratissima, the full-flowering stage of L. pinceana, and the four stages of L. yunnanensis) (Figure 5). L. gratissima occupied 10 special compounds, such as octanoic acid, ethyl ester, β-bourbonene, trans-isoeugenol, etc. L. pinceana had 13 special compounds, such as cyclosativene, limonene, (Z)-verbenol, etc. L. yunnanensis possessed 17 special compounds, such as β-pinene, phenylethyl alcohol, limonene oxide, etc. Previous research indicated that significant differences in floral scent composition were found in closely-related species [28], which is consistent with our study.

Figure 5.

Figure 5

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Principal component plots (PC1 vs. PC2 plots) for the volatiles of the full-flowering stage of L. gratissima, the full-flowering stage of L. pinceana, and the different flower stages of L. yunnanensis. (I) bud stage; (II) initial-flowering stage; (III) full-flowering stage; (IV) end-flower stage.

Reports have revealed that some characterized compounds were usually rich in the early stage of flower development; for example, linalool dominated the samples from younger-stage inflorescences in Protea species [29], and 1,8-cineole and (Z)-3-hexenol were only identified from essential oil in the bud stage of Rosa canina [30]. These characterized compounds could make the young organs healthier [31]. However, these compounds did not appear in L. yunnanensis or L. pinceana, and this might be because the content of these volatile compounds in a single flower was too low.

3. Materials and Methods

3.1. Plant Materials

Nine fresh early flowering inflorescences of three L. yunnanensis plants (separate distance among plants more than 100 m, three inflorescences per plant) were collected from Nujiang Lisu Autonomous Prefecture, Yunnan Province (26°21′ N; 98°49′ E) during its flourishing florescence on 9 November, 2016, and were inserted into deionized water before being transported to the Research Institute of Resources Insects, Chinese Academy of Forestry (RIRICAF) in Kunming. Subsequently, the inflorescences were preserved at 25 ± 1 °C. The flowers were classified into four groups according to their botanical characteristics (Figure 1) [4]: (I) bud stage: buds complete closed; (II) initial-flowering stage: semi-open petal; (III) full-flowering stage: completely open petals, observable yellow pistils and stamens; and (IV) end-flowering stage: petals and calyxes withered, stamens turned brown. Three replicates (three flowers from three inflorescences per replicate) were randomly conducted from different plants, and the results are means of three tests, including nine flowers.

3.2. Method

Volatile compounds of a complete flower were monitored using solid-phase microextraction (SPME). A total of five L. yunnanensis individuals were randomly selected and sampled for scent collection between 8:00 and 11:00; the method of scent collection was described by Li et al. [7]. The methods of scent collection and HS-SPME-GC-MS were consistent with the methods of L. pinceana [4] and L. gratissima [5]. Sampling by HS-SPME was performed by 100 µm polydimethylsiloxane (PDMS) SPME fiber. After the equilibration time (15 min), the fiber was exposed to the headspace of the capped glass vial (20 mL) to absorb volatile compounds for 40 min. The empty capped vial was used as the blank control.

A gas chromatograph-mass spectrometer (TRACE GC Ultra/ITQ900, Thermo Fisher Scientific, Inc., Waltham, MA, USA) coupled with a DB-5MS capillary column (5% diphenyl cross-linked 95% dimethylpolysiloxane, 30 m × 0.25 mm i.d. × 0.25 µm film thickness. Agilent J & W Scientific, Folsom, CA, USA) were used for the GC-MS analysis. The oven temperature was programmed at 40 °C for 2 min, increasing at a rate of 6 °C/min to 130 °C and then increasing at 15 °C/min to 280 °C for 5 min. The injector was performed in splitless mode for 1 min. Helium was the carrier gas at a flow rate of 1.0 mL/min. The mass spectrometer was operated in electron impact mode at an ionization voltage of 70 eV and ion source temperature of 250 °C, and the scan range was 50–650 amu.

3.3. Data Analysis

The GC-MS data were processed using the TF Xcalibur 2.1.0 software. Component identification was carried out using NIST 2008 mass spectral database and confirmed by the comparison of their linear retention index (LRI) with published data [15]. Identification of individual components could be confirmed by the comparison of both mass spectrum and GC retention data with those of authentic standards [32]. A series of n-alkane standards (C6-C19) (Accu Standard, New Haven, CT, USA) were analyzed under the same conditions to obtain LRI values for the volatile compounds. Peak areas were normalized as percentage and used to determine the relative amounts of the volatiles.

3.4. Statistical Analysis

The data were analyzed by one-way analysis of variance (ANOVA). Principal component analysis (PCA) and Bray–Curtis similarity (BCS) were carried out using PC-ORD for Windows (Version 5.0; MjM Software, Gleneden Beach, OR, USA).

4. Conclusions

HS-SPME coupled with GC-MS was adapted to determine the composition and content of floral scent emitted from different flower development stages of L. yunnanensis. The present investigation showed that 40 VOCs were identified in whole life flower-stages, and sesquiterpenes were the most abundant floral scent compounds. The amount of floral scent emission had the tendency to first ascend and descend in succession, reaching its peak level at the initial-flowering stage. However, the highest diversity of floral volatiles was detected at the full-flowering stage. Compared with the other two species of Luculia (L. pinceana and L. gratissima), the composition and relative content of floral scent were also different at four stages of the tree species. Furthermore, L. yunnanensis has a promising prospect for development as an essential oil source and for future breeding programs and cultivation, owing to the main compounds of the floral scent.

Acknowledgments

We thank Hua Zheng for assistance in GC-MS analysis and Haixia Wu for improving the English of this manuscript. This work was financially supported by Special Fund for Forest Scientific Research in the Public Welfare (201404705), Technology Innovation Talent Project of Yunnan Province (2016HB007) and the Fundamental Research Funds for the Central Non-profit Research Institution of CAF (riricaf201003M).

Author Contributions

Yuying Li, Hong Ma and Zhenghong Li conceived and designed the experiments; Yuying Li performed the experiment and wrote the manuscript; Youming Wan and Zhenghai Sun analyzed the data; Taiqiang Li edited the manuscript; Xiongfang Liu, Xiuxian Liu, Rui He and Yan Ma contributed to materials collection. All authors read and approved the final manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

Footnotes

Sample Availability: Samples of the compounds are not available from the authors.

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