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Characterization of the chemical composition of the essential oils from Annona emarginata (Schltdl.) H. Rainer 'terra-fria' and Annona squamosa L./Caracterizacao do Perfil quimico do oleo essencial de Annona emarginata (Schltdl.) H. Rainer 'terra-fria'e Annona squamosa L.


Annona is an important genus of the Annonaceae family, primarily because of its edible fruits. The genus Cananga (Annonaceae) includes species with industrially important essential oils (CHATROU et al., 2012).

Recent taxonomic studies using molecular techniques have reorganized the species and genera of the Annonaceae family. Several genera have been included in other genera (SURVESWARAN et al., 2010; ZHOU et al., 2010; COUVREUR et al., 2012). These reorganizations include the proposal of Rainer (2007) that the genus Rollinia A. St.-Hil. be treated as a synonym of the genus Annona. However, the scientific literature often refers to Rollinia A. St.-Hil. In the present study, Rollinia will be treated as a synonym of Annona.

Previous studies have shown that the species of the Annonaceae family exhibit a great diversity of substances produced by their secondary metabolism. These compounds include aromatic substances, phenolic acids, steroids, alkaloids, acetogenins, and essential oils (LEBOEUF et al., 1982; LIMA, 2007; REIS, 2011).

The term essential oil refers to a group of aroma-bearing substances resulting from secondary metabolism (SPERRY, 2000). These substances are often produced in secretory structures, such as glandular cells and oleiferous canals, or in other specific structures (SIMOES; MARIOT, 2003). These chemicals include, e.g., terpenes (monoterpenes and sesquiterpenes), phenylpropanoids, compounds containing nitrogen and sulfur, and aromatic compounds (BAKKALI et al., 2008). The essential oils have cytotoxic and phytotoxic effects (BAKKALI et al., 2008), which function to protect the plants against damage caused by arthropods; in addition, they are potentially very useful in medicine (LIMA et al., 2003; POTZERNHEIM et al., 2006; REGNAULT-ROGER et al., 2012). During the development of plants, secondary metabolism may be affected by numerous environmental factors, e.g., radiation, temperature, humidity, wind, and soil characteristics (WANG et al., 2012). According to Kamatou et al. (2008), several environmental conditions throughout the year affect the production, concentration, and biological activity of essential oils by plants. In nature, essential oils in plants serve important defensive functions, including bactericidal activity against Gram-positive and Gram-negative forms, antiviral and antifungal activity, insecticidal functions, and defense against herbivores. These compounds are also important for attracting dispersers of pollen and seeds and for repelling undesirable organisms (BAKKALI et al., 2008; RIVOAL et al., 2010). Several studies have been conducted to demonstrate the potential of essential oils in the pharmaceutical industry based on the functions of these oils in plant defense (EDRIS, 2007).

A number of studies have been performed in view of the pharmacological potential of the species of the Annonaceae family (OCAMPO; OCAMPO, 2006). The essential oil of A. coreacea Mart. has been found to exhibit antiprotozoan activity (SIQUEIRA et al., 2011). Muganza et al. (2012) conducted ethnopharmacological reviews of 33 plant species, including three species belonging to the Annonaceae family. These three species--Anonidium mannii Engl. & Diels, Enantia chlorantha Oliv., and Isolona hexaloba Engl. & Diels--were found to show anti-inflammatory activity affecting the blood vessels; antiprotozoan activity; and antimalarial activity and activity against headaches and appetite loss, respectively. Lima et al. (2012) have studied Annona cornifolia A. St.-Hil. and have noted that this species is a promising source of drugs for treating cancer because of its antioxidant and cytotoxic potential. Costa et al. (2009) have described the antimicrobial and antimalarial activities of A. foetida Mart. The biological activity cited for these three species of Annonaceae has been attributed to the effects of essential oils (COSTA et al., 2009; SIQUEIRA et al., 2011; LIMA et al., 2012).

The species A. emarginata 'terra-fria' is economically important because it is the most used rootstock in Brazil for cultivating atemoya, a plant whose fruit has great economic potential because of its organoleptic characteristics (TOKUNAGA, 2005). A. emarginata is highly resistant to stem borers, pests, and disease (KAVATI; WATANABE, 2010). The ecological resilience of the species in nature (rusticity) allows it to adapt to different nutritional conditions (BARON et al. 2013). In the Annonaceae family, essential oils occur not only in the leaves but also in other parts of the plant, such as the bark and roots, as previously shown by Boyom et al. (2011) and Muganza et al. (2012). A. squamosa (custard apple) and A. cherimola Mill. (cherimoya) are the species from which the atemoya hybrid originated. The potential biological activity of A. squamosa L. has been investigated. Seffrin et al. (2010) studied the seed extract of this species and found that it showed larvicidal activity against Trichoplusia ni. Other studies performed with the essential oil of the bark of A. squamosa L. have demonstrated its activity against Gram-positive bacteria. The author of such study has related this activity to the high percentage of caryophyllene oxide (29.38%) contained in the preparation. This form of biological activity has previously been described in the literature for such component (CHAVAN et al., 2006). The essential oil extracted from the leaves, bark, and stems of A. squamosa has been found to contain [alpha]-pinene, limonene, [beta]-cubebene, [beta]-caryophyllene, spathulenol, caryophyllene oxide, and [alpha]-cadinol as major components (THANG et al., 2012).

Although several studies on the Annonaceae family can be found in the literature, there are few reports about the chemical composition of the essential oil of the leaves of A. emarginata 'terrafria' and A. squamosa. These species are not only important to atemoya cultivation but may also show pharmacological activity of economic interest.

The goal of this study was to characterize the chemical composition of the essential oil extracted from leaves of A. emarginata 'terra-fria' and A. squamosa.


This study was conducted in a greenhouse with controlled temperature and humidity, located in the experimental area of the Instituto de Biociencias, Universidade Estadual Paulista, UNESP - Campus Botucatu, Departamento de Botanica, 48[degrees]24'35'' W, 22[degrees]49'10'' S, 850 m above sea level.

Specimens of A. emarginata 'terra-fria' and A. squamosa (custard apple) were obtained by germinating seeds from Sao Bento do Sapucai, 45[degrees]44'11" W, 22[degrees]41'18" S, 874 m above sea level. The seeds were sown in expanded polystyrene trays without dividers. During early development, the seedlings were transplanted to 10-L pots filled with a mixture of red earth, medium-textured vermiculite, and coconut fiber. The young plants then received weekly applications of Yogen[R] 3 nutrient solution containing 25% N, 6.5% P, 6.7% K, 0.053% Zn, 0.02% Co, 0.077% Mn, and 0.022% B (YOORIN[R]), as well as calcium nitrate, Ca[(N[O.sub.3]).sub.2] (HOAGLAND; ARNON, 1950). The nutrients provided were sufficient to ensure vegetative growth until 18 months after the transplantation to the pots, when leaves were collected for oil extraction.

The leaves of 10 A. emarginata 'terra-fria' plants and 15 A. squamosa plants were collected to obtain sufficient dry mass for essential oil extraction. The leaves were collected in the morning from 10:00 to 12:00 and then placed in a greenhouse (drying chamber) with forced-air heaters at 40[degrees]C for 48 hours until a constant dry mass was obtained. After the completion of drying, 80 g of the dry mass of the leaves was hydrodistilled in a Clevenger-type apparatus for 2 hours to extract the essential oils. The oils were separated from the aqueous phase with the addition of solvent dichloromethane (0.5 mL, Merck, chromatographic grade), and the solution was stored in amber glass bottles and kept in a freezer at -20[degrees]C prior to chemical analysis.

The chemical analysis of the essential oils was performed with gas chromatography coupled with electron-ionization mass spectrometry (70 eV) (GC-MS, Shimadzu, QP-5000). An OV-5 capillary column (Ohio Valley Specialty Chemical, Inc.; 30.0 m x 0.25 mm x 0.25 [micro]m) was used with the following operating characteristics: injector at 240[degrees]C, detector at 230[degrees]C, split injection (1/20), injection volume: 1 [micro]L of solution, ramp 60[degrees]C at 240[degrees]C, 3[degrees]C /min. The substances were identified by comparing their mass spectra with the GC-MS (Nist. 62 lib.) system database based on retention indices (ADAMS, 2007). The retention indices were obtained by injecting a standard mixture of hydrocarbons ([C.sub.9]-[C.sub.24]) with the same chromatography conditions described above and then applying the equation of Van Dool & Kratz (1963).


Eleven substances were identified in the essential oil of the leaves of A. emarginata 'terra-fria', and 10 components were identified in the oil of A. squamosa, as shown in Table 1. The major substances in the oil of both species were sesquiterpenes and monoterpenes. These results agree with the findings forA. glabra L., A. squamosa L., A. muricata L., and A. reticulata L. reported by Thang et al. (2012).

The essential oil of A. emarginata 'terra-fria' included five principal constituents: (E)-caryophyllene (29.29%), (Z)-caryophyllene (16.86%), [gamma]-muurolene (7.54%), [alpha]-pinene (13.86%), and tricyclene (10.04%) (Table 1). Five principal constituents were identified in the oil of A. squamosa L.: (E)-caryophyllene (28.71%), (Z)-caryophyllene (14.46%), camphene (18.10%), [alpha]-pinene (7.37%), and [beta]-pinene (8.71%) (Table 1). Accordingly, six components present in the oils of A. emarginata 'terra-fria' and A. squamosa L. should be highlighted: (E)-caryophyllene, (Z)-caryophyllene, [alpha]-humulene, camphene, [alpha]-pinene, and [beta]-pinene. Among the six components common to the two species, three are major components in both: (E)-caryophyllene, (Z)-caryophyllene, and [alpha]-pinene. Note that the percentages of (E)-caryophyllene and (Z)-caryophyllene were highly similar in both oils.

A previous evaluation of the composition of the essential oil of Rollinia leptopetala R. E. Fries showed that the following major components were present: cis-4-tujanol (17.37%), a-terpineol (8.42%), germacrene D (7.72%), bicyclogermacrene (22.47%), and trans-caryophyllene (6.63%) (synonymous with (A)-caryophyllene) (COSTA et al., 2008). A comparison of the composition of the essential oil of this species with that of the essential oil of A. emarginata 'terra-fria' shows that limonene, [alpha]-pinene, sabinene, trans-caryophyllene, and [alpha]-humulene were present in both oils. A comparison of the composition of the essential oil of R. leptopetala studied by Costa et al. (2008) with that of the essential oil of A. squamosa L. shows that [beta]-elemene, [alpha]-humulene, [alpha]-pinene, and trans-caryophyllene are common to both species. These observations show that [alpha]-pinene, trans-caryophyllene, and [alpha]-humulene occur in the essential oils of the three species R. leptopetala R. E. Fries, A. emarginata 'terra-fria', and A squamosa. Of these constituents, trans-caryophyllene is a major component and shows anti-inflammatory activity (FERNANDES et al., 2007).

Thang et al. (2012) evaluated the essential oils of A. glabra L., A. squamosa L., A. muricata L., and A. reticulata L., all grown in Vietnam. The authors found 48 components in the essential oil of A. squamosa L., among which [alpha]-pinene, [beta]-pinene, [alpha]-humulene, [gamma]-himachalene, camphene, and [beta]-elemene were also found in the essential oil of A. squamosa L. in the present study. It was also found (E)-caryophyllene, (Z)-caryophyllene, [alpha]-humulene, [gamma]-himachalene, [delta]-elemene, camphene, [alpha]-pinene, [beta]-pinene, [beta]-elemene, and longifolene in the essential oil of A. squamosa L. These results show that the essential oil of A. squamosa grown in Vietnam had a greater number of components than that of the plants of this species grown in Brazil in the present study. The comparison between the results from Brazil and Vietnam highlights that the major components of the essential oil of this species may vary, due to, e.g., to climatic conditions, soil, nutrition, and water availability (MORAIS, 2009). Although the composition of the essential oil of A. squamosa grown under different conditions may vary, a-pinene and [alpha]-humulene were found in both studies cited and have also been observed in studies of other plant species (CYSNE et al., 2005; KAMATOU et al., 2008; ZEBELO et al., 2012).

Among the components identified in the essential oil of both species of Annonaceae evaluated in this study, trans-caryophyllene has also been isolated from the essential oil of Cordia verbenacea and showed anti-inflammatory activity, offering an attractive alternative for treating inflammation (FERNANDES et al., 2007). Limonene may be used as a flavor and fragrance in food preparation, to reduce the fat content of chocolate and in the biological control of insects (ROBALO et al., 2007). [beta]-elemene has been shown to inhibit the growth of glioblastoma multiforme cells, found in a common and aggressive type of brain tumor (YOA et al., 2008). The substances [alpha]-pinene and [beta]-pinene have bactericidal activity (LEITE et al., 2007). Camphene is the precursor of theosemicarbazide, which has fungicidal activity (YAMAGUCHI et al., 2009). Therefore, this study identified essential oil components with known biological activity and additional components whose activity should be evaluated.


The analysis of the chemical constituents of the essential oils of the species A. emarginata 'terra fria' and A. squamosa identified monoterpenes and sesquiterpenes. Six substances were common to both species: [alpha]-humulene, (Z)-caryophyllene, (E)-caryophyllene, camphene, [alpha]-pinene, and [beta]-pinene. These two Annona species shared more than 50% of the same components of their essential oils.


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(1) (Trabalho 208-13) - Recebido em: 20-05-2013. Aceito para publicacao em: 29-01- 2014. V Congresso Internacional & Encontro Brasileiro sobre Annonaceae: do gene a exportacao (19 a 23 de Agosto de 2013). Botucatu-SP

(2) Master's student in Horticulture, Agronomy Sciences College, Universidade Estadual Paulista "Julio de Mesquita Filho" (UNESP) Botucatu Campus, Sao Paulo-SP, Brazil. Caixa Postal 237. E-mail address:

(3) Doctoral student in Botany, Biosciences Institute (IB), UNESP, Botucatu Campus, SP, Brazil; CP. 510. E-mail:

(4) Researcher at the P&D Center of Vegetable Genetic Resources, Agronomy Institute, Campinas, SP, Brazil. E-mail:

(5) Associate Professor of the Botany Department , Biosciences Institute, UNESP, Botucatu Campus, SP, Brasil; CP 510. E-mail:
TABLE 1--Chemical composition (%) of the essential oils of Annona
emarginata (Schltdl.) H. Rainer 'terra-fria' variety and Annona
squamosa L.

Substances            Annona emarginata   Annona        RI *   RI **
                      (Schltdl.) H.       squamosa L.
                      Rainer (%)          (%)

    Triciclene              10.04             --        926     926
  [alpha]-Pinene            13.86            7.37       933     939
     Camphene               1.33             18.10      947     953
     Sabinene               1.96              --        971     976
   [beta]-Pinene            1.83             8.71       976     980
   Ortho cimene             1.93              --        1021   1022
     Limonene               1.07              --        1027   1031
  [delta]-Elemene            --              1.15       1337   1339
  [beta]-Elemene             --              1.69       1391   1391
    Longifolene              --              5.64       1399   1402
 (Z)-Caryophyllene          16.86            14.46      1405   1404
 (E)-CaryophyUene           29.29            28.71      1418   1418
  [alpha]-Humulene          3.06             4.41       1445   1454
[gamma]-Himachalene          --              2.96       1476   1476
 [gamma]-Muurolene          7.54%             --        1475   1477
    Monoterpene            32.02%           34.18%       --     --
   Sesquiterpene           56.75%           59.02%       --     --
       TOTAL               88.77%            93.2        --     --

(*) ri--retention index of the sample (**) ri--retention index of
the literature (adams, 2007).
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Author:Campos, Felipe Girotto; Baron, Daniel; Marques, Marcia Ortiz Mayo; Ferreira, Gisela; Boaro, Carmen S
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Date:Feb 1, 2014
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