Abstract
The volatile profile of the edible vegetable Gynura bicolor [Gynura bicolor (Roxb. ex Willd.) DC] was analyzed using gas chromatography-mass spectrometry (GC-MS). Isocaryophyllene (23.2%), α-pinene (16.8%), α-humulene (9.1%), β-pinene (7.3%), and copaene (7.0%) were identified as the major compounds in the leaves. In the stems, α-pinene (27.1%), β-pinene (13.0%), isocaryophyllene (7.8%), β-myrceneb (7.8%), 1-undecene (5.7%), and copaene (5.3%) were the main components. G. bicolor grows best at 25 °C. When cultivated at different temperatures (20 to 35 °C in incements of 5 °C), the volatile profiles shifted. The proportion of isocaryophyllene was lower at 20 °C than at the other temperatures. The relative amounts of α-pinene and α-humulene were highest at 20 °C, whereas copaene was highest at 35 °C. Principal component analysis (PCA) was used to explore the correlation between volatile compounds identified from the vegetative tissues and temperature treatments. It reveals the same trend with the previous statements and the first principal component (PC1) and the second principal component (PC2) explains up to 90% of the variance. Experimental results revealed that both temperature and vegetative organ correlate with the volatile emission profile of G. bicolor.
G. bicolor is in the Asteraceae family and cultivated as a traditional vegetable (Hóng Fèng Cài) in various locations, including Taiwan, China, and Japan. Its leaves and stems are edible. The leaves of G. bicolor are characteristically green on the adaxial side and reddish-purple on the abaxial side. In Taiwan, there are large-leaved varieties with reddish stems and small-leaved varieties with greenish stems. G. bicolor is aromatic and has a high nutritional value because it is rich in iron, flavonoids, and anthocyanins. It is also used as a medicinal plant (Chao et al., 2015; Shimizu et al., 2009; Yoshitama et al., 1994).
A recent study identified 108 volatile components from the essential oil of G. bicolor (Miyazawa et al., 2016). Plant essential oils are complex mixtures of volatile constituents, and their major components are terpenoids, like isoprenoids (C5), monoterpenoids (C10), and sesquiterpenoids (C15), which are naturally occurring organic products (Holopainen and Gershenzon, 2010). Volatile compounds can protect plants from biotic and abiotic stresses by quenching stress-generated reactive oxygen species (ROS) and stabilizing cell membranes (Brilli et al., 2019; Loreto and Velikova, 2001; Velikova et al., 2011). Volatiles are stored in specialized tissues, such as resin ducts or glandular trichomes, and the stored volatiles may act as necessary signals for herbivores when selecting host plants (Mita et al., 2002). As plant defense mechanisms, volatile emissions can reduce herbivore feeding activity and inhibit the protease activities of pathogens (Baier et al., 2002; Niinemets et al., 2013). Volatile compounds also impart flavor and health benefits to humans (Ayseli and İpek Ayseli, 2016).
Plant volatile profiles and emissions are dependent on species, organs, developmental stages, and environmental conditions. Previous studies indicated that temperature affects both the synthesis and emission of volatile compounds (Copolovici and Niinemets, 2016; Grote et al., 2013; Guenther et al., 2012). Temperature can determine the gas–liquid phase partition of volatiles within the plant. A temperature increase converts more volatiles into the gas phase; thereafter, they can be emitted from the plant (Harley, 2013). For basil, temperature has significant effects on plant growth parameters that also affect the volatile oils of the fresh leaves (Chang et al., 2005). In young corn plants, the emission of terpenoids and indoles were high at 22 and 27 °C, respectively (Gouinguené and Turlings, 2002). In addition, the production and emission of volatiles can be detected at specific developmental stages and from different parts of the plant, such as leaves, roots, and flowers (Chiu et al., 2017; Possell and Loreto, 2013; Ren et al., 2014).
G. bicolor is an aromatic plant in the Asteraceae family and is cultivated as a vegetable in Taiwan. When compared with leafy vegetables grown in the same agricultural systems, G. bicolor is generally less affected by pests and diseases. In the field, high temperature (summer season) is a significant factor that limits plant growth and development of G. bicolor. We were curious to know whether its ability to produce certain volatile compounds suppresses pest and disease attacks. Therefore, this study aimed to determine the optimum temperature conditions for the growing season and to clarify the effects of temperature and vegetative parts on the volatile compound profiles and quality of G. bicolor.
Using a solid-phase microextraction (SPME) method coupled with GC-MS, we analyzed the volatile compound profiles of the leaves and stems of G. bicolor after growth at 25 ± 1 °C and the volatiles emitted by the leaves of G. bicolor grown under different temperatures in otherwise controlled environmental conditions. The released volatile compounds were grouped by different temperatures and the harvested organ by PCA.
Materials and Methods
Plant materials.
Apical shoots (≈20 cm) of the G. bicolor commercial cultivar Hóng Fèng Cài were transplanted to pots and grown for 14 d on an outdoor balcony (28 ± 3 °C) under shade. After 14 d, the plants were transferred to a growth chamber. The shoots were cultivated in the growth chamber for 50 d at 25 ± 1 °C with a 13-h light/11-h dark photoperiod and a light intensity of 129.0 ± 7.5 μmol⋅m−2⋅s−1 to obtain the material for the experiments.
Volatile compounds in vegetative parts of G. bicolor.
The two aerial parts of G. bicolor (leaves and stems) were separated at the petiole from the main stem and cut into pieces with scissors. The volatile compounds from 4.0 g of leaves/stems were placed into 20-mL headspace vials (20 mm outside diameter × 83 mm height × 15 mm inside diameter). The volatiles were extracted by headspace solid-phase microextraction (HS-SPME) for 25 min at 25 ± 3 °C with a 50/30 μm divinylbenzene/carboxen/polydimethylsiloxane (DVB/CAR/PDMS) fiber purchased from Supelco (Bellefonte, PA). The fiber was injected in a GC-MS injection unit. The sample extractions were conducted in triplicate.
Volatile profiles of plants grown at different temperatures.
Apical shoots of G. bicolor were transplanted to pots and grown for 14 d outdoors on a balcony under a shade canopy. The plants were transferred to different daytime temperature treatments (20, 25, 30, and 35 °C) in the growth chamber for 50 d. At the end of each temperature treatment, the following growth parameters were measured: plant height, plant fresh weight and dry weight, leaf area, number of nodes, and leaf thickness. Eight replicates were measured for the growth parameters. Fresh leaves (4.0 g) were collected and cut into pieces with scissors. These samples were placed in 20-mL headspace vials and extracted for 25 min to adsorb volatiles to the headspace SPME fiber. The fiber was injected in the injection unit of the GC-MS system. Four replicates were analyzed for each sample.
Analysis of GC-MS.
The GC-MS analyses were performed using an Agilent 7890B GC Plus coupled to a quadrupole mass spectrometry device (5977B MSD; Agilent, Palo Alto, CA) equipped with an HP-5MS column (30 m × 0.25 mm inside diameter; film thickness, 0.25 μm). The temperature was maintained at 250 °C in a splitless GC injector and detector. The oven temperature was maintained at 40 °C for 1 min, increase to 150 °C at 5 °C⋅min−1, maintained for 1 min, increased to 200 °C at 10 °C⋅min−1, and maintained for 11 min. The helium carrier gas flow rate was 1 mL⋅min−1 (Huang et al., 2010). Kovats indices were calculated for separate components relative to a series of C5-C25 n-alkanes (Schomburg and Dielmann, 1973). The constituents were identified by matching their spectra with those recorded in the Wiley 11/NIST 2018 MS library.
Statistical analysis.
The mean values of the experimental data were subject to an analysis of variance with the least significant difference test at the 1% level of significance using SAS (SAS Enterprise v 7.1; SAS, Cary, NC). The PCA was performed using all the volatile compounds identified from the vegetative tissues and temperature treatments. The PCA results were obtained using the prcomp command of the R package statistical software (Jolliffe and Cadima, 2016).
Results and Discussion
Volatile compounds in vegetative parts of G. bicolor.
Shoots of G. bicolor were grown at 25 °C and harvested separately as stems and leaves for analysis using GC-MS (Fig. 1). A total of 33 volatile compounds were identified, but had differing leaves and stems (Table 1). The main constituents in the leaves were isocaryophyllene (23.2%), α-pinene (16.8%), α-humulene (9.1%), β-pinene (7.3%), and copaene (7.0%); however, the major constituents in the stems were α-pinene (27.1%), β-pinene (13.0%), isocaryophyllene (7.8%), β-myrcene (7.8%), 1-undecene (5.7%), and copaene (5.3%). The identified volatile compounds of the stems and the leaves accounted for 94.4% and 85.9% of the total volatile content, respectively. The remaining volatile compounds in the stems (5.6%) and leaves (14.1%) were unknown (Table 1). According to the total ion chromatogram (TIC) of the volatiles, sesquiterpenes (isocaryophyllene) were the most abundant components in the leaves of G. bicolor. In the stems, monoterpene compounds (α-pinene) comprised the higher percentage (Fig. 1).
Total ion chromatogram (TIC) of the volatile compounds from the leaves (upper) and stems (lower) of G. bicolor grown at 25 °C in a growth chamber (peak labeled per numbering in Table 1).
Citation: HortScience horts 56, 8; 10.21273/HORTSCI15851-21
The mean percent peak area based on the TIC (TIC area %) of volatile compounds in two vegetative parts of G. bicolor as identified by GC-MS.
We performed a PCA to group the volatile compounds according to which part of the plant released them (Fig. 2). The two principal components (PCs) accounted for 99.7% of the observed variance, with PC1 explaining ≈99.1% of the variation. According to the PCA, isocaryophyllene and α-humulene were more highly emitted from the leaves, whereas α-pinene, β-pinene, and 1-undecene were more highly emitted from the stems. Miyazawa et al. (2016) reported that isocaryophyllene, α-pinene, and α-humulene were the three main compounds in the leaves of G. bicolor, whereas α-pinene, β-pinene, and myrcene were the three major components in the stems. These results were similar to the findings of our study. Isocaryophyllene is a major sesquiterpene in various essential oils from vegetable species and tends to accumulate in plant leaves (Vila et al., 1997; Zoghbi et al., 1995).
A principal component analysis of the correlation between volatile compounds and aerial vegetative tissues of G. bicolor (n = 3). 25CL indicates volatile compounds identified from the leaves grown at 25 °C in a growth chamber. 25CS indicates volatile compounds identified from the stems grown at 25 °C in a growth chamber. (See Supplemental Fig. 1. for a zoom into the volatile compounds with small loading values for the first and second principal components.)
Citation: HortScience horts 56, 8; 10.21273/HORTSCI15851-21
The emission of plant volatiles from vegetative parts is known to be involved in biotic and abiotic stresses. Isocaryophyllene and α-humulene (α-caryophyllene) are the isomers of β-caryophyllene; their biological effects include antimicrobial, antioxidative, and anticancer activities (Dahham et al., 2015). Previous experiments showed that β-caryophyllene from plant flowers serves as a defense against bacterial pathogens (Huang et al., 2012). The monoterpene pinene exists as two structural isomers (α-pinene and β-pinene) and are common in plant essential oils. Previous studies indicated that α-pinene, β-pinene, myrcene, limonene, and 3-carene have phytotoxic effects that inhibit insect feeding (López et al., 2011; Shi and Sun, 2010; Xu et al., 2014). These volatiles have several functions, such as signaling, resistance to oxidative stress, and defense against herbivores and pathogens (Dong et al., 2016).
Changes in the volatile profile with changes in temperature.
The plants of G. bicolor were grown under different temperature treatments in the growth chamber (Fig. 3). Plants grown at 25 °C showed the best values for growth indices such as plant height, leaf areas, node number, fresh weight, and dry weight (Table 2). Plants grown at 35 °C had smaller leaves, fewer nodes, and lighter fresh and dry weights, but the leaves were thicker (Table 2). The GC-MS analysis showed that the volatile compounds released from fresh leaves of G. bicolor changed with the ambient temperature (Table 3). The mean percent peak area was based on TIC (TIC area %) of volatile compounds. The total amounts of volatile compounds were not significantly different at 20 °C (86.0%), 25 °C (86.8%), 30 °C (85.1%), or 35 °C (85.6%), but other compounds in the leaves (13% to 15%) were unknown (Table 3). These results were similar to the effects of temperature on the emission of induced volatiles from corn plants (Gouinguené and Turlings, 2002). However, different temperatures could affect the number of monoterpenoids and sesquiterpenoids arising from the plant. Total monoterpenoids were significantly higher at moderate temperatures (20 and 25 °C) than at high temperatures (30 and 35 °C), whereas total sesquiterpenoid amounts were significantly increased at 30 and 35 °C (Table 3).
Potted G. bicolor plants were grown in growth chambers with different temperatures (20, 25, 30, and 35 °C, bar = 2.54 cm).
Citation: HortScience horts 56, 8; 10.21273/HORTSCI15851-21
Comparison of plant growth indices under different temperatures in a growth chamber.
The mean percent peak area was based on the TIC (TIC area %) of volatile compounds from fresh leaves of G. bicolor grown at different temperatures as identified by GC-MS.
Several factors, such as environmental and genetic factors and agricultural practices, can affect the volatile composition (Copolovici and Niinemets, 2016; Nurzyńska-Wierdak, 2012). Temperature is the key factor that influences the growth and development of plants as well as their volatiles content (Chang et al., 2005). Previous studies have shown that temperature affects the enzymes that synthesize volatile compounds. The duration of the temperature shift also influences the content of plant volatiles, with short-term changes enhancing the synthesis of volatiles and long-term changes reducing it (Kleist et al., 2012; Pazouki et al., 2016). In addition, temperature can induce changes in leaf structure and biomass, which can alter the physiological characteristics per unit area (Rasulov et al., 2015). Chang et al. (2005) reported that sweet basil grown at 25 °C had larger leaf areas, higher leaf fresh weights, and increased volatile oil content per unit weight than basil grown at other temperatures (15 and 30 °C). This study found that G. bicolor plants grown at 25 °C had larger leaf areas and higher leaf fresh weights than those grown at a higher temperature (35 °C) (Table 2). Additionally, plants growth at 35 °C had small and clustered leaves; this change might affect the generation of volatile components (Fig. 3).
The volatile compounds identified in the leaves of G. bicolor were mainly terpene hydrocarbons, such as monoterpenes and sesquiterpenes. The main volatiles were isocaryophyllene (16.0% to 23.3%), α-pinene (17.1% to 21.2%), copaene (6.5% to 13.4%), α-humulene (6.2% to 9.2%), and β-pinene (7.6% to 8.3%), as reported in previous studies (Miyazawa et al., 2016; Shimizu et al., 2009). Temperature did affect the relative content of these main volatiles. The proportion of isocaryophyllene was significantly lower at 20 °C (P < 0.01) than at other temperatures. In contrast, the relative amounts of α-pinene and α-humulene were highest at 20 °C, and that of copaene was highest at 35 °C (Table 3). The PCA was used to group the volatiles emitted by temperature treatments. The two main PCs explained ≈92.1% of the total variance in volatile emissions among the different temperatures. PC1 explained ≈60.6% of the variation and PC2 explained ≈31.5% of the variation. According to the PCA results, trans-3-hexenol and α-pinene were most influenced at 20 °C, whereas β-myrcene and aromadendrene were most influenced at 25 °C. The major volatiles were isocaryophyllene at 30 °C and copaene and δ-cadinene at 35 °C (Fig. 4). Gouinguené and Turlings (2002) reported that the relative β-caryophyllene emission quantity from corn plants was highest at 37 °C.
A principal components analysis of the correlation between volatile compounds from fresh leaves of G. bicolor and temperature treatment (n = 4). (See Supplemental Fig. 2. for a zoom into the volatile compounds with small loading values for the first and second principal components.)
Citation: HortScience horts 56, 8; 10.21273/HORTSCI15851-21
Previous studies showed that temperature determined the gas–liquid phase partition of the volatile compounds within plants according to Henry’s law constant (Harley, 2013; Niinemets et al., 2004). Additionally, temperature could change the stomatal conductance, which controls the emission of volatiles by diffusion resistance (Possell and Loreto, 2013). Recent studies showed that heat stress led to the release of sesquiterpenes and had selective effects on different monoterpenes in Solanum lycopersicum (Copolovici and Niinemets, 2016; Copolovici et al., 2012). For pine, emissions of sesquiterpenes were temperature-dependent and probably triggered as a direct stress response to high temperatures (>30 °C), whereas monoterpenes were more abundant at lower temperatures (Helmig et al., 2006, 2007). These results were similar to those of our study (Table 3). The terpenoids have a role in stabilizing membranes at high temperatures, which may protect plants from high temperatures (Singsaas, 2000).
The PCA is a type of linear transformation of a given data set with many variables to achieve lower dimensional projection of the given data set to preserve the maximum variance. The process of the PCA involves performing singular value decomposition (SVD) of the matrix to obtain eigenvalues and eigenvectors. Every eigenvector has a corresponding eigenvalue. PCs are new variables that are calculated by linear combinations of the given variables. PC1 has the maximum variance of all linear combinations and PC2 has the second highest variance. The eigenvector with the highest eigenvalue is the eigenvector of PC1, and the eigenvector with the second highest eigenvalue is the eigenvector of PC2. Figures 2 and 4 show a visualization of the variations in PC1 and PC2. The two PCs accounted for 99.7% and 92.1% of the variance of the observed datasets in Figs. 2 and 4, respectively.
G. bicolor is an aromatic leaf green that has a high nutraceutical value, partly because of its flavonoids and anthocyanins, which have various biological activities (Li et al., 2009; Wu et al., 2013). Furthermore, the volatile compounds of G. bicolor are mainly terpenes, which have functions such as antibacterial, cytoprotective, and pesticidal activities (Salehi et al., 2019). These components of G. bicolor may offer opportunities for developing biopesticides to reduce pests and disease damage in the field or for medicinal uses. This study of the volatile compounds of G. bicolor provides information that can help maximize the production of useful volatiles by regulating the cultivation temperature and carefully harvesting different vegetative organs for different volatile profiles.
Literature Cited
Ayseli, M.T. & İpek Ayseli, Y. 2016 Flavors of the future: Health benefits of flavor precursors and volatile compounds in plant foods Trends Food Sci. Technol. 48 69 77 doi: https://doi.org/10.1016/j.tifs.2015.11.005
Baier, P., Führer, E., Kirisits, T. & Rosner, S. 2002 Defence reactions of Norway spruce against bark beetles and the associated fungus Ceratocystis polonica in secondary pure and mixed species stands For. Ecol. Mgt. 159 73 86 doi: https://doi.org/10.1016/S0378-1127(01)00711-3
Brilli, F., Loreto, F. & Baccelli, I. 2019 Exploiting plant volatile organic compounds (VOCs) in agriculture to improve sustainable defense strategies and productivity of crops Front. Plant Sci. 10 264 doi: https://doi.org/10.3389/fpls.2019.00264
Chang, X., Alderson, P. & Wright, C. 2005 Effect of temperature integration on the growth and volatile oil content of basil (Ocimum basilicum L.) J. Hort. Sci. Biotechnol. 80 593 598 doi: https://doi.org/10.1080/14620316.2005.11511983
Chao, C., Liu, W., Wu, J. & Yin, M. 2015 Phytochemical profile, antioxidative and anti-inflammatory potentials of Gynura bicolor DC J. Sci. Food Agr. 95 1088 1093 doi: https://doi.org/10.1002/jsfa.6902
Chiu, Y.T., Chen, H.C. & Chang, C. 2017 The variation of Oncidium Rosy Sunset flower volatiles with daily rhythm, flowering period, and flower parts Molecules 22 1468 doi: https://doi.org/10.3390/molecules22091468
Copolovici, L., Kännaste, A., Pazouki, L. & Niinemets, Ü. 2012 Emissions of green leaf volatiles and terpenoids from Solanum lycopersicum are quantitatively related to the severity of cold and heat shock treatments J. Plant Physiol. 169 664 672 doi: https://doi.org/10.1016/j.jplph.2011.12.019
Copolovici, L. & Niinemets, Ü. 2016 Environmental impacts on plant volatile emission 35 59 Blande, J.D. & Glinwood, R. Deciphering chemical language of plant communication. Springer International Publishing Cham doi: https://doi.org/10.1007/978-3-319-33498-1_2
Dahham, S.S., Tabana, Y.M., Iqbal, M.A., Ahamed, M.B.K., Ezzat, M.O., Majid, A.S.A. & Majid, A.M.S.A. 2015 The anticancer, antioxidant and antimicrobial properties of the sesquiterpene β-caryophyllene from the essential oil of Aquilaria crassna Molecules 20 11808 11829 doi: https://doi.org/10.3390/molecules200711808
Dong, F., Fu, X., Watanabe, N., Su, X. & Yang, Z. 2016 Recent advances in the emission and functions of plant vegetative volatiles Molecules 21 124 doi: https://doi.org/10.3390/molecules21020124
Gouinguené, S.P. & Turlings, T.C.J. 2002 The effects of abiotic factors on induced volatile emissions in corn plants Plant Physiol. 129 1296 1307 doi: https://doi.org/10.1104/pp.001941
Grote, R., Monson, R.K. & Niinemets, Ü. 2013 Leaf-level models of constitutive and stress-driven volatile organic compound emissions 315 355 Niinemets, Ü. & Monson, R.K. Biology, controls and models of tree volatile organic compound emissions. Springer Netherlands Dordrecht doi: https://doi.org/10.1007/978-94-007-6606-8_12
Guenther, A.B., Jiang, X., Heald, C.L., Sakulyanontvittaya, T., Duhl, T., Emmons, L.K. & Wang, X. 2012 The model of emissions of gases and aerosols from nature version 2.1 (MEGAN2.1): An extended and updated framework for modeling biogenic emissions Geosci. Model Dev. 5 1471 1492 doi: https://doi.org/10.5194/gmd-5-1471-2012
Harley, P.C. 2013 The roles of stomatal conductance and compound volatility in controlling the emission of volatile organic compounds from leaves 181 208 Niinemets, Ü. & Monson, R.K. Biology, controls and models of tree volatile organic compound emissions. Springer Netherlands Dordrecht doi: https://doi.org/10.1007/978-94-007-6606-8_7
Helmig, D., Ortega, J., Duhl, T., Tanner, D., Guenther, A., Harley, P., Wiedinmyer, C., Milford, J. & Sakulyanontvittaya, T. 2007 Sesquiterpene emissions from pine trees -identifications, emission rates and flux estimates for the contiguous United States Environ. Sci. Technol. 41 1545 1553 doi: https://doi.org/10.1021/es0618907
Helmig, D., Ortega, J., Guenther, A., Herrick, J.D. & Geron, C. 2006 Sesquiterpene emissions from loblolly pine and their potential contribution to biogenic aerosol formation in the Southeastern US Atmos. Environ. 40 4150 4157 doi: https://doi.org/10.1016/j.atmosenv.2006.02.035
Holopainen, J.K. & Gershenzon, J. 2010 Multiple stress factors and the emission of plant VOCs Trends Plant Sci. 15 176 184 doi: https://doi.org/10.1016/j.tplants.2010.01.006
Huang, H.H., Wang, N.T., Kuo, X.K., Lin, L.Y., Wu, C.M. & Chen, H.C. 2010 Using solid phase microextraction method to evaluate volatile compounds in the fresh peel and in the essential oils extracted from the peel of ‘Liucheng’ orange (Citrus sinensis Osbeck) J. Taiwan Soc. Hort. Sci. 56 113 123 doi: https://doi.org/10.6964/JTSHS.201006.0113
Huang, M., Sanchez-Moreiras, A.M., Abel, C., Sohrabi, R., Lee, S., Gershenzon, J. & Tholl, D. 2012 The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-β-caryophyllene, is a defense against a bacterial pathogen New Phytol. 193 997 1008 doi: https://doi.org/10.1111/j.1469-8137.2011.04001.x
Jolliffe, I.T. & Cadima, J. 2016 Principal component analysis: A review and recent developments Philos. Trans.-Royal Soc., Math. Phys. Eng. Sci. 374 1 16 doi: https://doi.org/10.1098/rsta.2015.0202
Kleist, E., Mentel, T.F., Andres, S., Bohne, A., Folkers, A., Kiendler-Scharr, A., Rudich, Y., Springer, M., Tillmann, R. & Wildt, J. 2012 Irreversible impacts of heat on the emissions of monoterpenes, sesquiterpenes, phenolic BVOC and green leaf volatiles from several tree species Biogeosciences 9 5111 5123 doi: https://doi.org/10.5194/bg-9-5111-2012
Li, W.L., Ren, B.R., Zhuo, M., Hu, Y., Lu, C.G., Wu, J.L., Chen, J. & Sun, S. 2009 The anti-hyperglycemic effect of plants in Genus Gynura Cass Amer. J. Chin. Med. 37 961 966 doi: https://doi.org/10.1142/S0192415X09007430
Loreto, F. & Velikova, V. 2001 Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes Plant Physiol. 127 1781 1787 doi: https://doi.org/10.1104/pp.010497
López, M.F., Cano-Ramírez, C., Shibayama, M. & Zúñiga, G. 2011 α-Pinene and myrcene induce ultrastructural changes in the midgut of Dendroctonus valens (Coleoptera: Curculionidae: Scolytinae) Ann. Entomol. Soc. Amer. 104 553 561 doi: https://doi.org/10.1603/AN10023
Mita, E., Tsitsimpikou, C., Tsiveleka, L., Petrakis, P.V., Ortiz, A., Vagias, C. & Roussis, V. 2002 Seasonal variation of oleoresin terpenoids from Pinus halepensis and Pinus pinea and host selection of the scale insect Marchalina hellenica (Homoptera, Coccoidea, Margarodidae, Coelostonidiinae) Holzforschung 56 572 578 doi: https://doi.org/10.1515/HF.2002.087
Miyazawa, M., Nakahashi, H., Usami, A. & Matsuda, N. 2016 Chemical composition, aroma evaluation, and inhibitory activity towards acetylcholinesterase of essential oils from Gynura bicolor DC J. Nat. Med. 70 282 289 doi: https://doi.org/10.1007/s11418-015-0961-1
Niinemets, U., Kännaste, A. & Copolovici, L. 2013 Quantitative patterns between plant volatile emissions induced by biotic stresses and the degree of damage Front. Plant Sci. 4 262 doi: https://doi.org/10.3389/fpls.2013.00262
Niinemets, Ü., Loreto, F. & Reichstein, M. 2004 Physiological and physicochemical controls on foliar volatile organic compound emissions Trends Plant Sci. 9 180 186 doi: https://doi.org/10.1016/j.tplants.2004.02.006
Nurzyńska-Wierdak, R. 2012 Sweet basil essential oil composition: Relationship between cultivar, foliar feeding with nitrogen and oil content J. Essent. Oil Res. 24 217 227 doi: https://doi.org/10.1080/10412905.2012.676763
Pazouki, L., Kanagendran, A., Li, S., Kännaste, A., Rajabi Memari, H., Bichele, R. & Niinemets, Ü. 2016 Mono- and sesquiterpene release from tomato (Solanum lycopersicum) leaves upon mild and severe heat stress and through recovery: From gene expression to emission responses Environ. Exp. Bot. 132 1 15 doi: https://doi.org/10.1016/j.envexpbot.2016.08.003
Possell, M. & Loreto, F. 2013 The role of volatile organic compounds in plant resistance to abiotic stresses: Responses and mechanisms 209 235 Niinemets, Ü. & Monson, R.K. Biology, controls and models of tree volatile organic compound emissions. Springer Netherlands Dordrecht doi: https://doi.org/10.1007/978-94-007-6606-8_8
Rasulov, B., Bichele, I., Huve, K., Vislap, V. & Niinemets, Ü. 2015 Acclimation of isoprene emission and photosynthesis to growth temperature in hybrid aspen: Resolving structural and physiological controls Plant Cell Environ. 38 751 766 doi: https://doi.org/10.1111/pce.12435
Ren, J., Guo, S., Cheng, Q., Shen, Y. & Feng, H. 2014 Synergistic effects of CO2 and LED lighting on accumulation of terpenes in roots of Gynura bicolor Chin. Herb. Med. 6 228 236 doi: https://doi.org/10.1016/S1674-6384(14)60033-2
Salehi, B., Upadhyay, S., Erdogan Orhan, I., Kumar Jugran, A., Jayaweera, S.L.D., Dias, D.A., Sharopov, F., Taheri, Y., Martins, N., Baghalpour, N., Cho, W.C. & Sharifi-Rad, J. 2019 Therapeutic potential of α- and β-pinene: A miracle gift of nature Biomolecules 9 738 doi: https://doi.org/10.3390/biom9110738
Schomburg, G. & Dielmann, G. 1973 Identification by means of retention parameters J. Chromatogr. Sci. 11 151 159 doi: https://doi.org/10.1093/chromsci/11.3.151
Shi, Z.H. & Sun, J.H. 2010 Quantitative variation and biosynthesis of hindgut volatiles associated with the red turpentine beetle, Dendroctonus valens LeConte, at different attack phases Bull. Entomol. Res. 100 273 277 doi: https://doi.org/10.1017/S0007485309990228
Shimizu, Y., Imayoshi, Y., Kato, M., Maeda, K., Iwabuchi, H. & Shimomura, K. 2009 Volatiles from leaves of field-grown plants and shoot cultures of Gynura bicolor DC Flavour Fragrance J. 24 251 258 doi: https://doi.org/10.1002/ffj.1938
Singsaas, E.L. 2000 Terpenes and the thermotolerance of photosynthesis New Phytol. 146 1 2 doi: https://doi.org/10.1046/j.1469-8137.2000.00626.x
Velikova, V., Várkonyi, Z., Szabó, M., Maslenkova, L., Nogues, I., Kovács, L., Peeva, V., Busheva, M., Garab, G., Sharkey, T.D. & Loreto, F. 2011 Increased thermostability of thylakoid membranes in isoprene-emitting leaves probed with three biophysical techniques Plant Physiol. 157 905 916 doi: https://doi.org/10.1104/pp.111.182519
Vila, R., Mundina, M., Muschietti, L., Priestap, H.A., Bandoni, A.L., Adzet, T. & Cañigueral, S. 1997 Volatile constituents of leaves, roots and stems from Aristolochia elegans Phytochemistry 46 1127 1129 doi: https://doi.org/10.1016/S0031-9422(97)00400-7
Wu, C.C., Lii, C.K., Liu, K.L., Chen, P.Y. & Hsieh, S.L. 2013 Antiinflammatory activity of Gynura bicolor (Hóng Fèng Cài) ether extract through inhibits nuclear factor kappa B activation J. Tradit. Complement. Med. 3 48 52 doi: https://doi.org/10.1016/S2225-4110(16)30166-3
Xu, B.B., Liu, Z.D. & Sun, J.H. 2014 The effects of α-pinene on the feeding performance and pheromone production of Dendroctonus valens Entomol. Exp. Appl. 150 269 278 doi: https://doi.org/10.1111/eea.12161
Yoshitama, K., Kaneshige, M., Ishikura, N., Araki, F., Yahara, S. & Abe, K. 1994 A stable reddish purple anthocyanin in the leaf of Gynura aurantiaca cv. Purple Passion J. Plant Res. 107 209 214 doi: https://doi.org/10.1007/BF02344246
Zoghbi, M.G.B., Maia, J.G.S. & Luz, A.I.R. 1995 Volatile constituents from leaves and stems of Protium heptaphyllum (Aubl.) March. J. Essent. Oil Res. 7 541 543 doi: https://doi.org/10.1080/10412905.1995.9698581
The volatile compounds with small loading values of the PC1 and PC2 in two vegetative parts of G. bicolor.
Citation: HortScience horts 56, 8; 10.21273/HORTSCI15851-21
The volatile compounds with small loading values of PC1 and PC2 at different temperature conditions from fresh leaves of G. bicolor.
Citation: HortScience horts 56, 8; 10.21273/HORTSCI15851-21
