Tools to Tie: Flower Characteristics, VOC Emission Profile, and Glandular Trichomes of Two Mexican Salvia Species to Attract Bees
Abstract
:1. Introduction
2. Results
2.1. Floral Traits and Pollinator Monitoring
2.2. Glandular Indumenta and Volatile Organic Compounds (VOCs)
- -
- type A (Figure 3a,e, Table 2), present on leaves and inflorescences of both species (Figure 3h–m), is a typical peltate trichome, constituted by a basal epidermal cell, a neck cell, and by a 4 –cellular glandular head surrounded by a large subcuticular space in which the secretion is stored. The responses to all the lipophilic stains were positive as well as to Ruthenium Red and AlCl3, indicating the presence of terpenes and of major polysaccharide and flavonoid derivatives (Table 3).
- -
- type B (Figure 3b,e, Table 2) is a short capitate trichome, widespread on both the vegetative and the reproductive organs of both examined species (Figure 3h–m). It is constituted by a basal epidermal cell, a neck-stalk cell, and by a glandular head of 2–4 cells surrounded by a wide subcuticular space. Generally, these trichomes present an exclusive polysaccharide secretion released through the intact cuticle (Table 3).
- -
- type C (Figure 3c,f, Table 2) is a medium capitate trichome present only on the calyx of S. blepharophylla (Figure 3j). It is made up of one epidermal cell, one stalk cell, one neck cell and a globose head of 1–2 secretory cells surrounded by a storage chamber. The secretion tested positive to all the lipophilic stains, particularly the NADI reagent, indicating that they are exclusive terpene producers (Table 3).
- -
- type D (Figure 3d,g, Table 2) is a long capitate trichome occurring only on the calyx of S. greggii (Figure 3k). It is composed by 1–2 epidermal cells, two stalk cells, one neck cell and by a head of 2–4 secretory cells. The secreted material stored in the subcuticular space tested positive only to the lipophilic dyes, indicating the exclusive production of terpenes (Table 3).
3. Discussion
4. Materials and Methods
4.1. Plant Material, Floral Traits, and Pollinator Monitoring
4.1.1. Plant Material
4.1.2. Flower Traits
4.1.3. Pollinator Monitoring
4.2. Micro-Morphology of the Glandular Indumentum and Phytochemical Investigation (VOCs)
4.2.1. Scanning Electron Microscopy (SEM) and Light Microscopy (LM)
4.2.2. Headspace-Solid Phase Microextraction (HS-SPME) Analyses, Gas Chromatography–Mass Spectrometry (GC-MS) Analyses, and Peak Identification
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
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a | b | c | d | E | f | |
---|---|---|---|---|---|---|
S. blepharophylla | 17.79 1 (0.13) | 27.21 1 (0.42) | 10.60 1 (0.42) | 18.63 1 (0.38) | 16.61 1 (0.84) | 0.64 1 (0.05) |
S. greggii | 10.50 2 (0.26) | 24.66 2 (0.77) | 10.44 1 (0.39) | 16.40 2 (0.35) | 14.22 2 (0.38) | 0.73 2 (0.01) |
Trichome Morphotype | Leaf | Calyx | Corolla | ||||
---|---|---|---|---|---|---|---|
Abaxial | Adaxial | Abaxial | Adaxial | Abaxial | Adaxial | ||
S. blepharophylla | A | + | + | + | - | + | + |
B | + | + | + | + | + | + | |
C | - | - | + | - | - | - | |
S. greggii | A | + | + | + | + | + | + |
B | + | + | + | + | + | + | |
D | - | - | + | - | - | - |
Staining Procedure | Target Compounds | Observed Colour | S. blepharophylla | S. greggii | ||||
---|---|---|---|---|---|---|---|---|
Type A | Type B | Type C | Type A | Type B | Type D | |||
Nile Red | Neutral lipids | Golden-yellow | ++ | - | ++ | ++ | - | ++ |
Fluoral yellow-088 | Total lipids | Yellow to orange | ++ | - | ++ | ++ | - | ++ |
NADI reagent | Terpenes | Violet-blue | ++ | - | ++ | ++ | - | ++ |
FeCl3 | Polyphenols | Emerald-green | + | - | - | ++ | - | - |
AlCl3 | Flavonoids | Blue-green | + | - | - | + | - | - |
Ruthenium red | Acid polysaccharides | Pinkish to red | + | + | - | + | + | - |
Alcian blue | Muco- polysaccharides | Pale-blue | + | + | - | + | + | - |
Salvia blepharophylla | Salvia greggii | |||||
---|---|---|---|---|---|---|
l.r.i.a | Compounds | Relative Abundance (%) | Relative Abundance (%) | |||
Flowers | Leaves | Flowers | Leaves | |||
1 | 941 | α-pinene | 2.14 | -b | 2.27 | 3.23 |
2 | 954 | camphene | - | - | - | 0.57 |
3 | 982 | β-pinene | 2.44 | - | 14.32 | 24.96 |
4 | 993 | myrcene | - | - | 1.90 | - |
5 | 1005 | α-phellandrene | - | - | 0.45 | - |
6 | 1032 | limonene | - | 1.66 | 55.20 | - |
7 | 1034 | 1,8-cineole | 45.68 | - | - | 19.56 |
8 | 1052 | (E)-β-ocimene | - | 3.71 | - | - |
9 | 1062 | γ-terpinene | 0.36 | 0.86 | 0.22 | - |
10 | 1070 | cis-sabinene hydrate | - | - | 0.25 | 0.34 |
11 | 1076 | trans-linalool oxide (furanoid) | - | - | - | 0.89 |
12 | 1088 | terpinolene | - | 0.44 | 0.42 | - |
13 | 1090 | cis-linalool oxide (furanoid) | - | - | - | 0.67 |
14 | 1101 | linalool | - | 5.07 | - | 2.11 |
15 | 1102 | nonanal | 0.56 | - | - | - |
16 | 1104 | α-thujone | - | 0.41 | - | - |
17 | 1134 | cis-limonene oxide | - | - | 0.20 | - |
18 | 1140 | nopinone | 0.75 | 0.67 | - | - |
19 | 1141 | trans-limonene oxide | - | - | 3.63 | 0.08 |
20 | 1143 | camphor | 2.95 | - | - | 2.09 |
21 | 1156 | isoborneol | - | - | - | 0.17 |
22 | 1158 | sabinaketone | - | 0.47 | - | - |
23 | 1162 | trans-pinocamphone | - | - | 0.15 | 0.26 |
24 | 1167 | borneol | - | - | - | 0.26 |
25 | 1170 | δ-terpineol | - | - | - | 0.05 |
26 | 1178 | 4-terpineol | 1.23 | - | 0.19 | - |
27 | 1187 | (Z)-3-hexenyl-butyrate | 0.97 | - | - | - |
28 | 1192 | methyl salicylate | - | - | - | 0.14 |
29 | 1195 | γ-terpineol | - | - | 0.20 | - |
30 | 1202 | trans-dihydro carvone | - | - | 0.19 | - |
31 | 1204 | decanal | 0.63 | 1.88 | - | 0.23 |
32 | 1232 | isobornyl formate | 8.56 | 0.73 | - | - |
33 | 1241 | methyl carvacrol | 5.32 | 10.68 | 0.61 | 0.23 |
34 | 1259 | linalool acetate | - | 0.80 | - | - |
35 | 1272 | n-decanol | - | 0.08 | - | - |
36 | 1283 | (E)-anethole | - | 0.92 | - | - |
37 | 1285 | isobornyl acetate | 1.91 | - | - | - |
38 | 1300 | n-tridecane | - | 0.56 | - | - |
39 | 1340 | δ-elemene | - | 0.65 | - | - |
40 | 1351 | α-cubebene | - | - | - | 0.05 |
41 | 1368 | cyclosativene | - | - | 0.20 | 0.24 |
42 | 1376 | α-copaene | 0.86 | - | 0.53 | 2.6 |
43 | 1384 | β-bourbonene | 1.20 | 10.43 | 0.83 | 2.74 |
44 | 1390 | β-cubebene | 0.28 | - | 0.23 | 0.4 |
45 | 1391 | 7-epi-sesquithujene | - | 0.77 | - | - |
46 | 1392 | β-elemene | - | 1.05 | 0.15 | 0.55 |
47 | 1400 | n-tetradecane | - | 0.23 | - | - |
48 | 1403 | longifolene | 0.41 | - | - | 0.16 |
49 | 1409 | α-cedrene | 0.68 | 0.28 | - | - |
50 | 1420 | β-caryophyllene | 6.84 | 11.07 | 5.73 | 5.59 |
51 | 1429 | β-copaene | 0.48 | 1.33 | 0.39 | 0.65 |
52 | 1432 | β-gurjunene | - | - | 0.41 | 6.74 |
53 | 1438 | trans-α-bergamotene | - | 6.89 | - | - |
54 | 1439 | α-guaiene | - | - | - | 0.12 |
55 | 1441 | aromadendrene | - | - | 0.35 | 0.15 |
56 | 1445 | (Z)-β-farnesene | - | 6.82 | - | - |
57 | 1455 | (E)-geranyl acetone | 0.41 | 0.41 | - | - |
58 | 1456 | α-humulene | 0.76 | 2.34 | - | 0.45 |
59 | 1461 | alloaromadendrene | - | 1.40 | 0.16 | 0.93 |
60 | 1462 | cis-muurola-4(14),5-diene | - | 0.20 | 0.27 | 0.21 |
61 | 1470 | trans-cadina-1(6),4-diene | 2.65 | - | - | - |
62 | 1477 | γ-muurolene | 0.79 | - | 1.48 | 10.2 |
63 | 1480 | γ-curcumene | - | 0.06 | - | - |
64 | 1481 | germacrene D | 5.01 | 4.22 | 6.37 | 7.22 |
65 | 1490 | (E,Z)-α-farnesene | - | 0.80 | - | - |
66 | 1491 | trans-muurola-4(14),5-diene | - | - | 0.16 | - |
67 | 1492 | valencene | 0.46 | - | - | 0.51 |
68 | 1495 | bicyclogermacrene | - | 2.38 | - | - |
69 | 1496 | γ-amorphene | - | - | - | 0.13 |
70 | 1498 | α-muurolene | - | - | 0.30 | 1.08 |
71 | 1500 | n-pentadecane | - | 0.32 | - | - |
72 | 1502 | γ-patchoulene | 0.52 | 0.10 | 0.29 | - |
73 | 1507 | (E,E)-α-farnesene | - | 2.42 | 0.29 | 0.82 |
74 | 1513 | trans-γ-cadinene | 0.98 | - | 0.70 | 0.43 |
75 | 1524 | β-sesquiphellandrene | - | 1.73 | - | - |
76 | 1524 | δ-cadinene | 0.69 | - | 0.24 | 0.40 |
77 | 1549 | elemol | - | 0.25 | - | - |
78 | 1565 | (E)-nerolidol | - | 1.29 | - | - |
79 | 1575 | germacrene D-4-ol | - | - | - | 0.16 |
80 | 1576 | spathulenol | - | 2.16 | - | - |
81 | 1593 | (Z)-sesquilavandulol | - | 9.63 | - | - |
82 | 1595 | guaiol | - | - | - | 0.76 |
83 | 1600 | n-hexadecane | - | 1.28 | - | - |
84 | 1606 | humulene epoxide II | - | 0.14 | - | - |
85 | 1640 | epi-α-cadinol | - | - | 0.18 | - |
86 | 1693 | juniperol acetate | - | 0.33 | - | - |
87 | 1700 | n-heptadecane | - | 0.08 | - | - |
Monoterpene hydrocarbons | 4.94 | 6.67 | 74.78 | 28.76 | ||
Oxygenated monoterpenes | 66.40 | 18.83 | 5.42 | 26.71 | ||
Sesquiterpene hydrocarbons | 22.61 | 54.95 | 19.08 | 42.37 | ||
Oxygenated sesquiterpenes | - | 13.80 | 0.18 | 0.92 | ||
Phenylpropanoids | - | 0.92 | - | - | ||
Apocarotenoids | 0.41 | 0.41 | - | - | ||
Other non-terpene derivatives | 2.16 | 4.43 | - | 0.37 | ||
Total identified (%) | 96.52 | 100.00 | 99.46 | 99.13 |
Compound | Bee Species | Reference |
---|---|---|
1,8-Cineole | Euglossini, Bombus terrestris; Bombus vorticosus | [26,27,28,29] |
α-Pinene | Euglossini, Apis mellifera; Honeybees | [26,30] |
β-Pinene | Bombus; Honeybees | [31,32,33] |
Limonene | Bombus, Honeybees; B. terrestris; B. vorticosus | [29,31] |
β-Caryophyllene | Apis mellifera; | [29,34] |
α-Farnesene | [24] | |
(E,E)-α-Farnesene | B. terrestris; B. vorticosus; Apis mellifera | [29,31,35] |
Linalool | Colletidae bees; Apidae; Lasioglossum spp. | [36] |
(E)-β-Ocimene | Colletidae bees; Apidae; Lasioglossum spp. | [36] |
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Giuliani, C.; Giovanetti, M.; Lupi, D.; Mesiano, M.P.; Barilli, R.; Ascrizzi, R.; Flamini, G.; Fico, G. Tools to Tie: Flower Characteristics, VOC Emission Profile, and Glandular Trichomes of Two Mexican Salvia Species to Attract Bees. Plants 2020, 9, 1645. https://doi.org/10.3390/plants9121645
Giuliani C, Giovanetti M, Lupi D, Mesiano MP, Barilli R, Ascrizzi R, Flamini G, Fico G. Tools to Tie: Flower Characteristics, VOC Emission Profile, and Glandular Trichomes of Two Mexican Salvia Species to Attract Bees. Plants. 2020; 9(12):1645. https://doi.org/10.3390/plants9121645
Chicago/Turabian StyleGiuliani, Claudia, Manuela Giovanetti, Daniela Lupi, Marco Palamara Mesiano, Renata Barilli, Roberta Ascrizzi, Guido Flamini, and Gelsomina Fico. 2020. "Tools to Tie: Flower Characteristics, VOC Emission Profile, and Glandular Trichomes of Two Mexican Salvia Species to Attract Bees" Plants 9, no. 12: 1645. https://doi.org/10.3390/plants9121645