Agrarian Academic Journal

agrariacad.com

doi: 10.32406/v7n5/2024/34-44/agrariacad

 

Bioecology of Tuta absoluta Meyrick 1917 (Lepidoptera: Gelichiidae) on tomato under greenhouse in the oasis of El-Oued (Algeria). Bioecologia de Tuta absoluta Meyrick 1917 (Lepidoptera: Gelichiidae) em tomateiro em estufa no oásis de El-Oued (Argélia).

 

Azzeddine Haddad^1,2*, Bachir Khezzani^1,2, Hanane Guerinik^1,2

 

^1*- Department of Agronomy, Faculty of Natural and Life Sciences, University of El Oued, PO Box 789, El Oued 39000, Algeria. E-mail: azzeddine-haddad@univ-eloued.dz

^2- Laboratory of Biodiversity and Biotechnology Applications in Agriculture, Faculty of Natural and Life Sciences, University of El Oued, El Oued 39000, Algeria. E-mail: bachirkhezzani05@gmail.com, haguerinik@hotmail.fr

 

Abstract

 

Tomato cultivation in the northern Mediterranean and North African countries is considered one of the most important factors on which the agricultural economy depends, given the spread of the Tuta absoluta insect in tomato fields and greenhouses and its impact on economic yield. The aim of this research is to study the dynamics of this pest on two varieties of tomatoes, the most cultivated, (Dawson and Tavira) in the southern region of the Algerian Sahara. Monitoring of the population dynamics of this pest was carried out during the 2021-2022 campaign. The results were as follows: During the period from 01/14/2022 until 03/18/2022 there was a progressive and significant increase in the numbers of adults ranging from 19.5 individuals/trap to 146.2 individuals/trap which is a peak recorded on 03/18/2022 on the Tavira variety in the Hassi Khalifa station. From this date and until the end of the phenological cycle of tomato cultivation on 04/01/2022 where a progressive decrease in the numbers of individuals was recorded due to a negative correlation with the high temperatures 35°C recorded during this period. While no correlation with the humidity levels recorded. Four (4) generations have been recorded. In conclusion, rational control of this pest can be achieved through biological methods to maintain the sustainability of these sensitive areas.

Keywords: Arid region. Inventory. Leaf miner. Saharan. Solanaceous.

 

 

Resumo

 

O cultivo de tomate nos países do norte do Mediterrâneo e do norte da África é considerado um dos fatores mais importantes dos quais depende a economia agrícola, dada a disseminação do inseto Tuta absoluta em campos de tomate e estufas e seu impacto no rendimento econômico. O objetivo desta pesquisa é estudar a dinâmica desta praga em duas variedades de tomate, as mais cultivadas (Dawson e Tavira) na região sul do Saara argelino. O monitoramento da dinâmica populacional desta praga foi realizado durante a campanha de 2021-2022. Os resultados foram os seguintes: Durante o período de 14/01/2022 a 18/03/2022, houve um aumento progressivo e significativo no número de adultos variando de 19,5 indivíduos/armadilha para 146,2 indivíduos/armadilha, que é um pico registrado em 18/03/2022 na variedade Tavira na estação Hassi Khalifa. A partir desta data e até o final do ciclo fenológico do cultivo do tomateiro em 01/04/2022 onde foi registrada uma diminuição progressiva no número de indivíduos devido a uma correlação negativa com as altas temperaturas de 35°C registradas durante este período. Enquanto nenhuma correlação com os níveis de umidade registrados. Quatro (4) gerações foram registradas. Em conclusão, o controle racional desta praga pode ser alcançado por meio de métodos biológicos para manter a sustentabilidade dessas áreas sensíveis.

Palavras-chave: Região árida. Inventário. Bicho-mineiro. Saara. Solanáceo.

 

 

Introduction

 

Tuta absoluta (Lepidoptera: Gelechiidae) originates from the South American tropics but has become a major invasive pest of tomato and other Solanaceae crops worldwide (LIU et al., 2023). South American tomato pinworm, Tuta absoluta (Meyrick, 1917) (Lepidoptera: Gelechiidae) also known as the tomato leaf miner is an oligophagous pest associated with solanaceous crops (SRIVASTAVA et al., 2018). Tuta absoluta is a major threat to tomato production, causing losses ranging from 80% to 100% when not properly managed. Early detection of T. absoluta’s effects on tomato plants is important in controlling and preventing severe pest damage on tomatoes (LOYANI et al., 2021). However, the El-Oued region in South-East Algeria is considered a major economic center where the production of vegetable crops, particularly tomatoes in greenhouses, occupies very large areas (D.A.S., 2020). In recent years, numerous pests have attacked these crops, particularly Tuta absoluta (Meyrick 1917), which causes considerable damage. The pest is native to Peru, where it is a serious pest on solanaceous vegetables, its infestation is being noticed both in protected and open fields (SHASHANK et al., 2015). Since the initial detection, this has become the most serious pest causing severe damage to tomato in many areas (SRIDHAR et al., 2014). It is solanaceous oligophagous pest, primary host is tomato although potato, brinjal, common bean and other wild solanaceous family plants are also convenient hosts (KALLESHWARASWAMY et al., 2015). Since 2008, considerable damage has occurred across all the market gardening regions of Algeria. Caused by the introduction of the tomato leaf miner Tuta absoluta, reported for the first time in the Mostaganem region (BADAOUI and BERKANI, 2010). According to Loyani et al. (2021) and Allache et al. (2012), they mentioned that Tuta absoluta is a very destructive insect pest with a strong preference for tomato plants, stems and fruits both in greenhouses and in the open field. It has the potential for expansion not only geographically, but also on other plants (DESNEUX et al., 2010). However, Drouai et al. (2016) reported that ten plants of cultivated and spontaneous types were identified as host plants for Tuta absoluta, these plants belong to the Solanaceae, Amaranthaceae and Fabaceae families. And four spontaneous species have not been reported as host plants for T. absoluta which are (Chenopodium rubrum L., Chenopodium bonus-henricus L., Spinacia oleracea L. & Beta vulgaris L.). Furthermore, the extent of the damage caused by this insect is very considerable (BADAOUI and BERKANI, 2010). In El-Oued, Saharan region and which confirms the South American leaf miner mainly attacks tomatoes (CHENNOUF et al., 2021). According to Badaoui and Berkani et al. (2010), who indicated that this lepidopteran is a dangerous pest for tomatoes. This pest, which is limited to tomatoes, can attack and cause damage to other nightshades. This has been reported in Argentina (PEREYRA et al., 2006). The pest is native to Peru, where it is a serious pest on solanaceous vegetables, its infestation is being noticed both in protected and open fields (SHASHANK et al., 2015). It is solanaceous oligophagous pest, primary host is tomato although potato, brinjal, common bean and other wild solanaceous family plants are also convenient hosts (KALLESHWARASWAMY et al., 2015). High reproductive potential of pest, short generation time, multivoltine character and its aggressive nature are the reasons for its easy adaptability in the new locations (ETTAIB et al., 2016). Chemical insecticides are the only method applied as control strategies against pinworm by the tomato growers which increased cost of cultivation and poor-quality produce (KUMAR et al., 2020). In order to limit its damage, a study of the population dynamics of T. absoluta is crucial. This part is a contribution to the study of the bioecology of this micro lepidopteran on two varieties of tomato in a greenhouse on two farms in the El-Oued region where the bioclimatic stage is part of the Saharan zones. The objective of this work is to understand the dynamics of Tuta absoluta on tomato crops and the impact of climatic factors on its evolution in the northern Algerian Sahara.

 

Material and methods

 

Location of the study: The test took place in two stations chosen in the El Oued region and were used to carry out this monitoring. The stations are Hassi Khalifa and Guemar. The selected stations are considered to be representative of the widely distributed biotopes in the region.

 

Hassi Khalifa Site

 

Is located 35 km northeast of the town of El Oued at Lambert coordinates (33° 31’ 12.68’’ N., 7° 2’ 25.00’’ E.). Its altitude is 57 m.

 

Guemar Site

 

The station is part of an agricultural area, located near the town of Guemar, (33° 29′ 37.27” N., 6° 40′ 20.69” E.). At altitude is 69 m.

 

Plant material

 

The two chosen stations produce crops in greenhouses, notably tomato cultivation (Solanum lycopersicum L). In each station two greenhouses, measuring 50m x 10m, and with an area of 500m², are devoted to the study: Two varieties of tomatoes in a greenhouse were grown in pots in a nursery protected by insect proof on 09/15/2021 for the follow-up to Tuta absoluta. The varieties cultivated and subject to the study are: Tavira and Dawson: a greenhouse for the Dawson variety, a greenhouse for the Tavira variety which are hybrid varieties and considered among the most used varieties in this region. Tomatoes grow well in warm, fertile, well-drained soils, and in areas exposed to direct sunlight for a period of at least 6 hours per day (VAN DER STRATEN et al., 2011). Phytosanitary treatments were not applied.

 

Characteristics of the Dawson variety

 

The Dawson variety has heart-shaped fruits, with a flame-red center; oranges streaked with yellow, its flesh is full, juicy, very fine and particularly seedless, it is rich in sugar and has a good flavor, presenting a very good yield with late fruits, from 80 to 100 days and large sizes of a mass of 300 g to 1 kg depending on the growing conditions (A.T.I.V.I.C., 2021).

 

Characteristics of the Tavira variety

 

She is originally from Holland. Round fruit, slightly flattened, weighing 180 to 200 gr and orange-red in colour with a round green collar, juicy and dense, very fragrant and sweet, comes in a bouquet of 06 to 07 fruits and is harvested 60 to 80 days earlier (A.T.I.V.I.C., 2021).

 

Soil characteristics

 

The soil is sandy loamy, permeable. The basic manure is composed of 120 tonnes/ha of farm manure, 200 kg/ha of 45% super phosphate and 200 kg/ha of sulphate of potash. Maintenance manure is applied in the form of soluble fertilizers during irrigation. The macro-elements (N, P, K) are provided according to the balances (20, 10, 10) and (11, 40, 11) with varying quantities depending on the progress of the stages of development of the crop. Planting took place on September 15 and 16, 2021 with planting distances in single rows of 40 cm between plant bases and 90 cm between rows. Maintenance work was limited to pruning the axillary buds of the tomato, removing leaves from the base of the plants and old leaves of the two varieties and manual weeding. Hygro-thermometers were placed in the middle of each greenhouse, to record, every week during the sampling period, the temperature and the surrounding relative humidity level inside these greenhouses.

 

Sex pheromone trap

 

To estimate pest populations and determine the optimal timing for interventions. The use of sex attractant traps provides good indications of the time of appearance of butterflies and the size of the pest population (VRENOZI et al., 2020). The use of sex attractant traps provides good indications of the time of appearance of butterflies and the size of the pest population (VRENOZI et al., 2020, p. 141).  On this basis, we have chosen this method in order to: Detect the beginning of flight of T. absoluta butterflies, Assess the life cycle of the tomato leaf miner and determine the number of generations. We used six sex traps: two traps in each greenhouse. The Hassi Khalifa site and the Guemar site. The traps used are of the Delta (Triangular) type with its accessories (glue plate and pheromone). The traps were provided to us by the Plant Protection Station of Ain-Touta in Batna. To capture male adults, use Delta type pheromone traps at the entrance and exit of each greenhouse at a height of 1.20 m from the ground. The traps are installed from the end of November 2021. The aim of trapping adults using sex pheromones was to detect the start of flights and at the same time the evolution and fluctuations of adult populations in order to to determine the number of generations of T. absoluta. The counting of catches is carried out every week from 03/12/2021 until 01/04/2022 end of the phenological cycle of the plant which corresponds to the beginning of April when the crop generally begins to dry (Figure 1) and (Figure 2). Concerning the sampling of leaves which allowed us in this study to identify the stages of the pest encountered only on leaves. Therefore, leaf sampling was carried out periodically for the enumeration of eggs, larvae and pupae. Monitoring is carried out as follows: Every week 20 leaves are taken randomly from 20 plants. These leaves were brought back to the laboratory and observed under the binocular magnifying glass. On each leaf the eggs, larvae and pupae are counted. Note that no phytosanitary treatment was applied so as not to hinder the arrival of probable native natural antagonists. The counting of male adults is carried out every week in the greenhouse on the two different varieties of tomato in each of the two sites. Individuals of Tuta absoluta captured in a greenhouse are carefully collected in plastic bottles with a little 70° alcohol. Each bottle has a label indicating the date and location of sampling.

 

Statistical analysis

 

A data normality test was performed. It revealed that the data followed the normal distribution at 95% for adults, 99% for eggs and 95% for larvae and pupae. An analysis of variance was carried out to test the difference between the means per month of the different stages of T. absoluta at the 5% threshold. An LSD test was carried out to compare the monthly averages of each stage (Xlstat 16).

 

Results and discussion  

 

The first flight of T. absoluta adults was detected in the pheromone traps on 12/24/2021 at the Hassi Khalifa station on the Dawson variety (3 male adults captured) (Figure 1); while for the Tavira variety the first adult captured was on December 17, 2021 at the Hassi Khalifa station (Figure 2). Tomato is attacked by several pests, howsoever a leaf mining insect i.e., Tuta absoluta of the lepidopteran group is a serious pest of tomato throughout the globe (YADAV et al., 2022). The South American tomato pinworm, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae), has invaded most Afro-Eurasian countries and is threatening worldwide tomato production (DESNEUX et al., 2022). Four generations of T. absoluta were recorded, on the two varieties and at the two sites during the phenological cycle of tomato cultivation. The best time for mating started in the morning (EL-RAHMAN et al., 2015). From the months of October, November and January, the average number of adults captured by traps recorded on leaves was very low (Figure 1 and 3). The counting of winged individuals of T. absoluta, during the sampling period, at the study stations, show that the number of the population increased gradually during the months of February and March, for the two varieties of tomato planted. in greenhouse, Tavira and Dawson. The averages of the highest numbers of the T. absoluta population, 146.2 individuals counted on tomatoes in greenhouses, on the Tavira variety, on March 18, 2022 at the Hassi khalifa station, while the Guemar station has recorded 111 individuals counted on tomato variety Tavira for the same date (Figure 2). Four overlapping generations were counted, which does not agree with Chennouf et al. (2021), who reported that the overall population dynamics of T. absoluta shows three (3) successive generations within six months. which is the tomato growing cycle. A maximum of 18 individuals were counted; 21,01, 39 and 90,03 individuals on the Tavira variety and 3, 20,04, 45,43 and 73,15 on the Dawson variety respectively in the two sites. Our results are consistent with those previously reported by Elouissi (2016), who reported that captures are low when temperatures are extreme (10°C) with hygrometry that is too low or too high. Catchments are maximum when temperatures vary from 20 to 25°C and when humidity is between 50 and 70% with the exception of the dates of 02/10 and 02/17/2014 (ETTAIB et al., 2016). On the other hand, the influence of winds in general, and sirocco in particular, on the catches of adults of T. absoluta was verified. Catches were significantly reduced when the sirocco appeared. This appears to be due to high temperatures above 40°C and humidity below 40% (ELOUISSI, 2016). The flight curves of adults of the tomato leaf miner T. absoluta represent the average numbers of captures of male adults at the two stations by use of sexual traps using water traps with a specific pheromone diffuser at the greenhouse level. studied of the two varieties Tavira and Dawson, during the 2021-2022 season (Figure 1 and 2) indicate that the temporal evolution of the number of adults of T. absoluta captured following variations in temperatures and humidity levels at the level of greenhouses studied at the two stations (Figure 3) that there is no correlation with ambient humidity. However, the correlations between number of adults and ambient temperatures (Figure 3) show that there are positive and weak correlations with temperatures, this agree with the quotes from Allache et al. (2020) who indicated that its results obtained on monitoring the flight curves of adults of the tomato leaf miner in the south-eastern region of Algeria showed that climatic factors (temperatures and humidity) had influence on the number of populations of T. absoluta in greenhouses (ALLACHE et al., 2020). However, Elouissi (2016) mentioned that population dynamics seem closely linked to weather conditions. The presence of this pest was observed throughout the development cycle of the tomato crop, this agrees with the results obtained by Allache et al. (2012), who noticed the presence of T. absoluta throughout the development cycle. of tomato cultivation. We found 3 solanaceous weeds in the vicinity of T. absoluta-infested fields in Arumeru District: Solanum incanum L., Datura stramonium L. and Nicandara physalodes (L.) Gaertn. None of these species were infested by T. absoluta (SMITH et al., 2018).

 

Figure 1 – Average number of adults of Tuta absoluta captured in traps on the Dawson variety. 2021-2022 campaign.

 

However, Pepper (Capsicum annuum L.) and African eggplant (Solanum aethiopicum L.) were not affected by T. absoluta (SMITH et al., 2018). Tuta absoluta distinguishes between different host plants. He showed a preference in descending order for tomato, black nightshade, eggplant, potato, and bell pepper (EL-RAHMAN et al., 2015). However, no natural enemies of this pest have been observed. This pushes us to develop the introduction of biological control by introducing exotic natural enemies in the El-Oued region in order to be able to limit the number of populations of T. absoluta existing on the different varieties of tomato cultivation. Drouai et al. (2016) indicated that it is necessary to develop biological control through the use of plant extracts to limit the impact of the pest T. absoluta to levels that are considered economically tolerable and for the preservation of the ‘environment. During the entire tomato growing cycle, adult populations of T. absoluta went through four generations. While to Kaouthar et al. (2010), who noted that T. absoluta completes four generations on this same crop in a greenhouse while in its area of origin in Latin America this pest develops 12 generations per year (BARRIENTOS et al., 1998). We see four peaks where the maximums were recorded on 12/24/2021 (18 adults), 02/11 (51.7 adults), 02/25/2022 (84.2 adults) and finally on the 18th. /03/2022 (146.2 adults) (Figure 2). From February, temperatures gradually increase in the greenhouse, and we see that there is an increase in the numbers of the different stages of T. absoluta. The average number of adults recorded is between 2 to 18 ind./trap of adults in the months of December/January and 90.3 ind./trap of adults at the beginning of March and 87.25 ind./trap of adults around mid-March; However, the number of populations sees a gradual decline during the end of March and the beginning of April, due to very significant increases in temperatures which reach an average of 35°C. This decrease in the number of winged adults towards the end of the crop cycle could be explained by the intense heat recorded during this period in March and early April. According to the statistical analysis, the evolution of this number during the growing season is highly significant (F = 67.23; p = 0.0000; df = 4). The analysis of variance showed that the number of eggs, larvae and pupae showed significant differences during the spring period (Table 1), (F = 62.02; p = 0.0000; df = 4). The numbers of individuals recorded on the Dawson variety for the two stations showed low averages compared to the averages recorded on the Tavira variety, during the phenological cycle of tomato cultivation where 3 ind./traps were recorded. end of December so that it reaches 24.6 ind./trap on 12/31/2021. 89.16 ind./trap recorded on 02/25/2022 and the peak with 119.24 ind./trap recorded on 03/18/2022 at the Hassi Khalifa station on the Tavira variety. The eggs are tiny and invisible to the naked eye, measuring less than a millimetre. They have a cylindrical shape and have a yellowish color, often located on the underside of the leaves and at the level of young tender stems and sepals of young fruits. The larvae measure a few millimetres long. First yellowish in color, then greenish to pink, they dig galleries on the aerial organs of the tomato. However, the chrysalis stage takes place either inside the galleries or on the surface of the plant. While adults measuring 4mm to 6mm. The leaves of its host plants are the preference of this pest, followed by the sepals and stem. However, the apical part of the plants is more attractive for females to lay than the middle and basal parts (EL-RAHMAN et al., 2015). According to El-Rahman et al. (2015), who indicated that the larvae are sensitive to light and prefer dark areas. The butterfly has nocturnal habits and greater activity at dawn and morning and dusk, however, it rests among the leaves of the host plant during the day (EL-RAHMAN et al., 2015). The larvae show great sensitivity to various sugars to varying degrees, thanks to their taste receptors and distinguish between host plants and different chemicals (EL-RAHMAN et al., 2015).

 

Figure 2 – Average number of Tuta absoluta adults captured in traps on the Tavira variety. 2021-2022 campaign.

 

Table 1 – Evolution of the averages per month of all stages of the Tuta absoluta population (± standard deviation). Means in the same column followed by the same letter are not significantly different at the 5% threshold.

Month	Averages / month (± Standard errors)
	Eggs	Larvae	Chrysalises	Adults
October 2021	0	0	0	(0,24±0,26) a
November 2021	0	0	0	(0,29±0,38) a
December 2021	(0,22±0,25) a	(0,10±0,26) a	(0,11±0,31) a	(6,68±0,42) a
January 2022	(6,32±0,34) a	(21,14±0,37) b	(2,33±0,33) b	(16,23±0,41) b
February 2022	(36,42±0,41) b	(46,44±0,96) c	(10,41±0,55) c	(50,55±0,40) c
March 2022	(16,1±0,21) c	(8,01±0,21) d	(3,12±0,21) d	(94,13±0,21) d

 

In tomato crops grown under polyhouse conditions or in open condition it cause 50-100% loss (SRIVASTAVA et al., 2018). However, Agricultural protected facilities (APFs) such as greenhouses and plastic tunnels may provide thermal conditions that allow the survival of T. absoluta in temperate zones with cold winters (LIU et al., 2023). In order to support research on Tuta absoluta, it is essential to determine its infestations on nightshades and particularly on tomato cultivation in the Saharan regions.

 

Figure 3 – Correlation of the numbers of Tuta absoluta adults at the two sites, Hassi khalifa and Guemar, with temperatures (Fig. a, c, e and f) and ambient humidity (fig. b, d, f and h), during the 2021-2022 agricultural campaign.

 

Conclusion

 

The study of the greenhouse pest Tuta absoluta (Meyrick) on tomato crops in the El Oued region using pheromone traps shows that the overall population dynamics reveal (4) four generations that were recorded during the vegetative cycle of tomato cultivation. Tuta absoluta in the adult state remains present throughout the vegetative cycle and at all sampling dates, on both Tavira and Dawson varieties. The number of Tuta absoluta adults on both greenhouse tomato varieties is low during the autumn period, although greenhouse nursery tomato planting began in mid-September. The overall number of adults becomes significant from mid-February on both the Tavira and Dawson varieties. The number of adults is low on the Dawson tomato variety compared to the Tavira variety. Tuta absoluta showed a weak positive correlation with increasing ambient temperatures. However, no correlation was recorded with hygrometry. Egg, larval and pupal stages showed significant differences between the different means during the spring period.

 

Conflicts of interest

 

The author declares no conflicts of interest regarding the work presented here.

 

Authors’ contribution

 

Azzeddine Haddad – conceptualization, methodology, data acquisition, data curation, visualization, writing riginal draft; Bachir Khezzani – methodology, visualization, writing original draft, writing review & editing; Hanene Guerinik – methodology, investigation, acquisition of data, data curation, writing original draft, writing review & editing.

 

Funding

 

None.

 

Acknowledgements

 

The authors would like to thank the head of the Agricultural Sciences Department for his help as well as Mr. Lâabed Y. Plant Protection Inspector at the National Institute of Plant Protection (I.N.P.P.) who provided us with the pheromone capsules of Tuta absoluta (Meyrick 1917) And we are very grateful to the farmers of Hassi Khalifa Site and Guemar site (El-Oued Oasis), who welcomed us and facilitated our field work in their greenhouse.

 

References

 

A.T.I.V.I.C. Algerian Technical Institute of Vegetable and Industrial Crops. Collection of Valuable Technical Sheets for Vegetable and Industrial Crops. 2021. https://itcmi-dz.org/fiches-techniques/

ALLACHE, F.; DEMNATI, F. Monitoring and population changes of Tuta absoluta (Meyrick, 1917) on tomato under greenhouse conditions in an arid expanse of south-eastern Algeria. Acta Agriculturae Slovenica, v. 115, n. 2, p. 409-416, 2020. https://doi.org/10.14720/aas.2020.115.2.324

ALLACHE, F.; MOHAMED, A. H.; OSMANE, I.; NAILI, L.; DEMNATI, F. Suivi de l’évolution de la population de Tuta absoluta Meyrick (Gelichiidae), un nouveau ravageur de la tomate sous serre à Biskra (sud-est d’Algérie).  Entomologie Faunistique – Faunistic Entomology, v. 65, p. 149-155, 2012. https://popups.uliege.be/2030-6318/index.php?id=2453&file=1&pid=2441

BADAOUI, M. I.; BERKANI, A. Morphologie et comparaison des appareils génitaux de deux espèces invasives Tuta absoluta Meyrick 1917 et Phthorimaea operculella Zeller 1873 (Lepidoptera: Gelechiidae). Entomologie Faunistique – Faunistic Entomology, v. 63, n. 3, p. 191-194, 2010. https://popups.uliege.be/2030-6318/index.php?id=1913&file=1&pid=1906

BADAOUI, M. I.; BERKANI, A.; LOTMANI, B. Les entomopathogènes autochtones, nouvel espoir dans le contrôle biologique de Tuta absoluta Meyrick 1917 (Lepidoptera: Gelechiidae) en Algérie. Entomologie Faunistique – Faunistic Entomology, v. 63, n. 3, p. 165-169, 2010. https://popups.uliege.be/2030-6318/index.php?id=1892&file=1&pid=1882

BARRIENTOS Z, R.; APABLAZA, H. J.; NORERO, S. A.; ESTAY, P. P. Threshold temperature and thermal constant for development of the South american tomato moth, Tuta absoluta (Lepidoptera: Gelechiidae). Ciencia e Investigación Agraria, v. 25, p. 133-137, 1998. https://www.scirp.org/reference/referencespapers?referenceid=2083140

CHENNOUF, R.; SAGGOU, H.; GUEZOUL, O.; BRAHMI, K.; DOUMANDJI-MITICHE, B. Etude de la bioécologie du Tuta absoluta Meyrick (Lepidoptera, Gelechiidae) dans la région de Ouargla (Sahara septentrional, Algérie). Revue des BioRessources, v. 11, n. 1, p. 85-92, 2021. https://dspace.univ-ouargla.dz/jspui/bitstream/123456789/27447/1/B110110.pdf

D.A.S. Directorate of Agricultural Services of the El-Oued Region.  Final annual report on greenhouse crop monitoring, 2019 – 2020 campaign. 2020. https://rhinotenders.com/companies/company/dsa-direction-des-services-agricoles-de-la-wilaya-d-el-oued-k

DESNEUX, N.; WAJNBERG, E.; WYCKHUYS, K. A. G.; BURGIO, G.; ARPAIA, S.; NARVÁEZ-VASQUEZ, C. A.; GONZÁLEZ-CABRERA, J.; RUESCAS, D. C.; TABONE, E.; FRANDON, J.; PIZOL, J.; PONCET, C.; CABELLO, T.; URBANEJA, A. Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. Journal of Pest Science, v. 83, p. 197-215, 2010. https://doi.org/10.1007/s10340-010-0321-6

DESNEUX, N.; HAN, P.; MANSOUR, R.; ARNÓ, J.; BRÉVAULT, T.; CAMPOS, M. R.; CHAILLEUX, A.; GUEDES, R. N. C.; KARIMI, J.; KONAN, K. A. J.; LAVOIR, A.-V.; LUNA, M. G.; PEREZ-HEDO, M.; URBANEJA, A.; VERHEGGEN, F. J.; ZAPPALÀ, L.; ABBES, K.; ALI, A.; BAYRAM, Y.; CANTOR, F.; CUTHBERTSON, A. G. S.; VIS, R.; ERLER, F.; FIRAKE, D. M.; HADDI, K.; HAJJAR, M. J.; ISMOILOV, K.; JAWORSKI, C. C.; KENIS, M.; LIU, H.-T.; MADADI, H.; MARTIN, T.; MAZIH, A.; MESSELINK, G. J.; MOHAMED, S. A.; NOFEMELA, R. S.; OKE, A.; RAMOS, C.; RICUPERO, M.; RODITAKIS, E.; SHASHANK, P. R.; WAN, F.-H.; WANG, M.-H.; WANG, S.; ZHANG, Y.-B.; BIONDI, A. Integrated pest management of Tuta absoluta: practical implementations across different world regions. Journal of Pest Science, v. 95, p. 17-39, 2022. https://doi.org/10.1007/s10340-021-01442-8

DROUAI, H.; MIMECHE, F.; ZEDAM, A.; MIMECHE, H.; BELHAMRA, M.; BICHE, M. New floristic records of Tuta absoluta Meyrick 1917, in Zibans’s Oasis (Biskra Algeria). Journal of Entomology and Zoology Studies, v. 4, n. 6, p. 130-132, 2016. https://www.entomoljournal.com/archives/?year=2016&vol=4&issue=6&ArticleId=1332

ELOUISSI, M. Contribution à l’étude de la bio écologie des populations de la mineuse de la tomate Tuta absoluta (Lepidoptera, Gelechiidae) en vue de l’optimisation de son contrôle dans la région de Mascara. 189p. Thèse (Doctorat) – Université Abdelhamid Ibn Badis, Mostaganem, Algeria, 2016. http://e-biblio.univ-mosta.dz/bitstream/handle/123456789/1084/CD26.pdf?sequence=1&isAllowed=y

ETTAIB, R.; BELKADHI, M. S.; BELGACEM, A. B.; AOUN, F.; VERHEGGEN, F.; MEGIDO, R. C. Effectiveness of pheromone traps against Tuta absoluta. Journal of Entomology and Zoology Studies, v. 4, n. 6, p. 841-844, 2016. https://www.entomoljournal.com/archives/?year=2016&vol=4&issue=6&ArticleId=1424

KALLESHWARASWAMY, C. M.; MURTHY, M. S.; VIRAKTAMATH, C. A.; KUMAR, N. K. K. Occurrence of Tuta absoluta (Lepidoptera: Gelechiidae) in the Malnad and Hyderabad-Karnataka regions of Karnataka, India. Florida Entomologist, v. 98, n. 3, p. 970-971, 2015. https://doi.org/10.1653/024.098.0326

KAOUTHAR, L. G.; MANEL, S.; MOUNA, M.; RIDHA, B. Lutte intégrée contre la mineuse de la tomate, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) en Tunisie. Entomologie Faunistique – Faunistic Entomology, v. 63, n. 3, p. 125-132, 2010. https://popups.uliege.be/2030-6318/index.php?id=1775&file=1

KUMAR, Y. P.; RAMADEVI, A.; CHARAN, G. S.; KUMAR, M. S.; RAGHUVEER, M.; POSHADRI, A. Field assessment on management of South American pin worm, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in tomato. Journal of Entomology and Zoology Studies, v. 8, n. 5, p. 360-363, 2020. https://www.entomoljournal.com/archives/?year=2020&vol=8&issue=5&ArticleId=8224

LIU, X.-X.; YANG, M.; ARNÓ, J.; KRITICOS, D. J.; DESNEUX, N.; ZALUCKI, M. P.; LU, Z. Protected agriculture matters: year-round persistence of Tuta absoluta in China where it should not. Entomologia Generalis, v. 4, n. 2, p. 279-287, 2023. https://doi.org/10.1127/entomologia/2023/1784

LOYANI, L. K.; BRADSHAW, K.; MACHUVE, D. Segmentation of Tuta absoluta’s damage on tomato plants: a computer vision approach. Applied Artificial Intelligence, v. 35, n. 14, p. 1107-1127, 2021. https://doi.org/10.1080/08839514.2021.1972254

PEREYRA, P. C.; SÁNCHEZ, N. E. Effect of two solanaceous plants on developmental and population parameters of the tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotropical Entomology, v. 35, n. 5, p. 671-676, 2006. https://doi.org/10.1590/S1519-566X2006000500016

SALAMA, H. S. A. E-R.; ISMAIL, I. A.-K.; FOUDA, M.; EBADAH, I.; SHEHATA, I. Some ecological and behavioral aspects of the tomato leaf miner Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Ecologia Balkanica, v. 7, n. 2, p. 35-44, 2015. http://web.uni-plovdiv.bg/mollov/EB/2015_vol7_iss2/035-044_eb.15129.pdf

SHASHANK, P.; CHANDRASHEKAR, K.; MESHRAM, N. M.; SREEDEVI, K. Occurrence of Tuta absoluta (Lepidoptera: Gelechiidae) an invasive pest from India. Indian Journal of Entomology, v. 77, n. 4, p. 323-329, 2015. https://doi.org/10.5958/0974-8172.2015.00070.X

SMITH, J. D.; DUBOIS, T.; MALLOGO, R.; NJAU, E.-F.; TUA, S.; SRINIVASAN, R. Host range of the invasive tomato pest Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) on solanaceous crops and weeds in Tanzania. Florida Entomologist, v. 101, n. 4, p. 573-579, 2018. https://doi.org/10.1653/024.101.0417

SRIDHAR, V.; CHAKRAVARTHY, A. K.; ASOKAN, R.; VINESH, L. S.; REBIJITH, K. B.; VENNILA, S. New record of the invasive South American tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in India. Pest Management in Horticultural Ecosystems, v. 20, n. 2, p. 148-154, 2014. https://www.researchgate.net/publication/304312970_New_record_of_the_invasive_South_American_tomato_leaf_miner_Tuta_absoluta_Meyrick_Lepidoptera_Gelechiidae_in_India

SRIVASTAVA, R. M.; REDDI, M. S.; SINGH, R. P.; SRIVASTAVA, P. Report of invasive pest Tuta absoluta (Meyrick) from Tarai area of North Western Himalayan region (Uttarakhand). Indian Journal of Entomology, v. 80, n. 4, p. 1719-1722, 2018. http://doi.org/10.5958/0974-8172.2018.00224.9

VAN DER STRATEN, M. J.; POTTING, R. P. J.; VAN DER LINDEN, A. Introduction of the tomato leafminer Tuta absoluta into Europe. Proceedings of the Netherlands Entomological Society Meeting, v. 22, p. 23-30, 2011. https://www.researchgate.net/publication/254842507_Introduction_of_the_tomato_leafminer_Tuta_absoluta_into_Europe

VRENOZI, B.; BURMAN, J.; TOSHOVA, T. B.; TARMANN, G. M. The application of sex attractant traps for studying the Zygaenidae (Lepidoptera) fauna of Albania. Entomologist’s Gazette, v. 71, n. 2, p. 135-148, 2020. https://doi.org/10.31184/G00138894.712.1751

YADAV, S. P. S.; BHATTARAI, S.; GHIMIRE, N. P.; YADAV, B. A review on ecology, biology, and management of a detrimental pest, Tuta absoluta (Lepidoptera: Gelechiidae). Journal of Agriculture and Applied Biology, v. 3, n. 2, p. 77-96, 2022. https://doi.org/10.11594/jaab.03.02.02

 

 

 

Received on April 8, 2024

Returned for adjustments on October 16, 2024

Received with adjustments on October 26, 2024

Accepted on November 16, 2024

Agrarian Academic Journal

agrariacad.com

doi: 10.32406/v7n5/2024/19-33/agrariacad

 

In vitro antioxidant, antimicrobial and antidiabetic properties of the organic fraction of distillate of Salvia hispanica seeds. Propriedades antioxidantes, antimicrobiana e antidiabéticas in vitro da fração orgânica do destilado de sementes de Salvia hispanica.

 

Ibtissem Rahmoune^1,2*, Samira Karoune^2*, Clara Azzam³, Somia Saad², Abdelhamid Foughalia², Madani Sarri⁴, Farid Chebrouk⁵, Hana Abidat^1,2, Mohamed Seif Allah Kechebar²

 

^1- Laboratory of Functional Ecology and Environment, Larbi Ben M’Hidi, University of Oum El Bouaghi, Algeria. E-mail: rahmoune.ibtissam@univ-oeb.dz

^2- Center for Scientific and Technical Research on Arid Regions – CRSTRA, Omar El Bernaoui, Biskra, Algeria. E-mail: karounesamira@yahoo.fr

^3- Cell Research Department, Field Crop Research Institute, Agricultural Research Center, Giza, Egypt.

^4- Department of Nature and Life Sciences, Faculty of Sciences, M’sila University, M’sila, Algeria. E-mail: madani.sarri@univ-msila.dz

^5- Center for Scientific and Technical Research in Physico-Chemical Analyzes, Tipaza, Algeria.

 

Abstract

 

This work aims to test in vitro biological properties and phytochemical composition of the organic fraction of distillate of Salvia hispanica seeds. Twenty-five bioactive compounds were identified, constituting 90.40% of the total organic fraction. The chemical composition of organic fraction revealed that fatty acids were the main component at 78.93%, followed by steroids (6.95%) and tocophérol (1.87%). The organic fraction showed interesting antioxidant activity for DPPH, DMSO, ABTS, PHE and FRAP tests. Furthermore, the in vitro enzyme inhibitory activity against α-amylase exhibited the best activity (IC₅₀ = 34.97 ± 0.68 μg/mL). The results indicated that organic fraction displayed good antimicrobial effect.

Keywords: Chia seeds. Phytochemical analysis. Biological properties. GC/MS. Fatty acids.

 

 

Resumo

 

Este trabalho tem como objetivo testar propriedades biológicas in vitro e composição fitoquímica da fração orgânica do destilado de sementes de Salvia hispanica. Vinte e cinco compostos bioativos foram identificados, constituindo 90.40% da fração orgânica total. A composição química da fração orgânica revelou que os ácidos graxos foram o principal componente em 78.93%, seguidos por esteroides (6.95%) e tocoferol (1.87%). A fração orgânica mostrou atividade antioxidante interessante para os testes DPPH, DMSO, ABTS, PHE e FRAP. Além disso, a atividade inibitória enzimática in vitro contra α-amilase exibiu a melhor atividade (IC₅₀ = 34.97 ± 0.68 μg/mL). Os resultados indicaram que a fração orgânica apresentou bom efeito antimicrobiano.

Palavras-chave: Sementes de chia. Análise fitoquímica. Propriedades biológicas. GC/MS. Ácidos graxos.

 

 

Introduction

 

Salvia hispanica, also known as Chia or Spanish sage, is a food crop newly recognized for its pharmacological and nutritional properties that may have enormous application potential in food systems (GRANCIERI et al., 2019). It is an annual herbal plant from the Lamiaceae family, native to Central America (CAHILL, 2003).

Currently, Chia seeds are becoming increasingly popular in modern diets due to their essential nutrients and health-enhancing activity that have been recognized in some of their components, including their high dietary fiber content (OLIVOS-LUGO et al., 2010), carbohydrates (LIN et al., 1994), fatty acids (ISHAK et al., 2021), proteins (SANDOVAL-OLIVEROS & PAREDES-LÓPEZ, 2013), and high levels of phenolic compounds (MARTÍNEZ-CRUZ & PAREDES-LÓPEZ, 2014) that display various physiological function properties, including antioxidant, antibacterial, anticancer, and anti-inflammatory.

Oxidation, a fundamental metabolic process, is responsible for breaking down organic molecules to produce energy and generating reactive oxygen species (ROS) as byproducts. While these ROS are natural byproducts, they can lead to oxidative stress, a factor implicated in a range of human diseases, including diabetes, cancer, skin pigmentation problems, and obesity (KOEPKE et al., 2008). Type 2diabetes, a prevalent chronic disease, is regulated by oxidative stress through molecular mechanisms (FOLLI et al., 2011). In this condition, the body resists insulin, a hormone crucial for blood sugar regulation. This resistance leads to high blood sugar levels, which is known as hyperglycemia.

The activity of digestive enzymes, particularly α-amylase, significantly influences blood sugar levels. It breaks down complex carbohydrates, such as starch, into simpler sugars, like glucose, which can then be absorbed by the body and released into the bloodstream to provide energy for cells and tissues. Therefore, inhibiting α-amylase activity can reduce the release of glucose into the blood stream (TARLING et al., 2008). The combination of antioxidants and α-amylase suppression holds promise for the treatment of type 2 diabetes, cancer, and obesity.

Several natural compounds, such as polyphenols, fatty acids, tocopherols, and steroids, are present in seeds, fruits, vegetables, and certain herbs. These compounds possess antioxidant properties, α-amylase inhibitory activity, and antibacterial effects. They have enormous potential in preventing and treating various diseases, thus underscoring the importance of exploring natural therapies in medical research.

Based on the reasons indicated above, this research was conducted with the aim of in vitro evaluation of the antioxidant, antidiabetic, and antibacterial properties of the organic fraction distillate from S. hispanica seeds (OFSH) extracted using a Clevenger distillation apparatus. The composition of the organic fraction was examined using GC/MS. The antioxidant properties were evaluated using seven assays, including ABTS, DPPH, PHE, FRAP, alkaline- DMSO, CUPRAC, and PRAC. The antidiabetic activity was evaluated by the α-amylase enzyme. Further, the antimicrobial effect was studied using the disc diffusion method against eight bacterial species and one pathogenic yeast.

 

Materials and methods

 

Organic fraction extraction

 

One hundred grams of powdered Salvia hispanica seeds (purchased from Algeria) were distilled using traditional hydro distillation with 1L of distilled water for four hours using a Clevenger-type apparatus. The resulting fraction yield was 1.9 g. Then this fraction was stored in screw-capped glass vials in a refrigerator at – 4°C. The yield was estimated based on the dry weight of the sample.

 

Free radical scavenging test (DPPH)

 

The antioxidant capacity of the OFSH was tested using DPPH test as published (BOUCHOUKH et al., 2019). Briefly, a 96-well microplate was used to mix 40 μL of diluted fraction dissolved in DMSO at different concentrations (from 12.5 to 800 μg/mL) with 160 μL of a 0.1 mM DPPH solution. At a wavelength of 517 nm, the absorbance was read using a Multiskan Sky Plate reader from Singapore (5111700DP) after incubating the mixture for 30 minutes in the darkness at room temperature. BHT was used as a positive reference. The DPPH inhibition (%) was calculated using the following equation (1). The IC₅₀, or sample concentration that lowered 50% of free radicals was obtained by plotting the acquired inhibitions against the sample concentrations.

(1) DPPH+ scavenging ability (%) = (A₀ – A₁)/A_0,

where A₀ and A₁ are the absorbance of control and fraction at 30 min, respectively.

 

Free radical scavenging test (ABTS)

 

The capacity of ABTS to scavenge free radicals was evaluated using the described procedure (RE et al., 1999). Briefly, 5 mL of 7.7 mM ABTS solution was blended with 5 mL of 2.45 mM potassium peroxide to produce the free radical cation ABTS+. The resulting mixture was diluted with H₂O until it exhibited an absorption of 0.7± 0.02 at a wavelength of 734 nm after incubation for 16 hours in the darkness at room temperature. Then, 40 µL of OFSH at different concentrations (from 12.5 to 800µg/mL) were combined with 160 µL of fresh ABTS+ mixture. At 734 nm, the absorbance was recorded after 10 minutes of incubation in the darkness at room temperature. BHT was used as a positive control. The radical scavenging ratio of ABTS+ was determined based on the formula (2) below:

(2) ABTS+ scavenging ability (%) = (A_b – A_f)/A_b,

where A_b and A_f are the absorbance of control and fraction at 10 min, respectively.

 

Ferric reducing power test

 

The FRAP test involves the reduction of iron oxide to ferrous ions. The potential reduction of OFSH was estimated using the published protocol (OYAIZU, 1986). Briefly, 40 μl of phosphate buffer solution (PBS: 0.2 M with a pH=6.6), 50 μL of potassium ferricyanide (C₆FeK₃N₆, 1%) were mixed with 10 μL of OFSH at various concentrations (from 3.125 to 200 μg/mL). After leaving the mixture in the incubator at 50°C for 20 min, 50 µL of 10% trichloroacetic acid (TCA) solution and 10 µl of 0.1% iron chloride were added to the sample and supplemented with 40 µl of H₂O. At a wavelength of 700 nm, the absorbance was recorded, and the results are presented as A_0.5 values (µg/mL) using ascorbic acid as a positive reference.

 

Superoxide radical test

 

Superoxide radical activity was assessed using the method described (KUNCHANDY & RAO, 1990). Briefly, in a 96-well microplate, 40 μL of OFSH at different concentrations (from 12.5 to 800 μg/ml) were mixed with130 μL of alkaline DMSO (20 mg of sodium hydroxide in 1 mL of H₂O and supplement with DMSO to 100 mL), followed by 30 μl of nitroblue tetrazolium (1 mg/mL). At the wavelength of 560 nm, the absorbance was recorded directly at 560 nm. The findings were expressed as BHT equivalent used as a positive control. The formula below (3) was used to calculate the percentage of superoxide inhibition:

(3) % inhibition = (Ac − At / Ac) × 100; A control absorbance is denoted by (Ac), while OFSH absorbance is denoted by (At).

The resulting inhibitors were graphed against the concentrations of the sample, and the graphs were used to calculate the IC₅₀, which is the concentration that reduces superoxide by 50%.

 

Cupric reducing antioxidant activity

 

The CUPRAC test was conducted to assess the antioxidant capacity of OFSH to reduce copper in the presence of neocuproine, using the published protocol (APAK et al., 2004). The test involves measuring the ability of antioxidants to reduce Cu⁺² to Cu⁺. In a microplate 96 well, 60 µL of ammonium acetate solution (1 M, pH 7), 50 µL of neocuproine and 50 µL of copper chloride (CuCl₂) solution (10 mM) were added to 40 µl of OFSH at various concentrations (from 12.5 to 400 µg/mL). The reaction was incubated for 1h, and the absorption was recorded at a wavelength of 450 nm. A_0.5 (µg/mL) was used to determine antioxidant activity results.

 

Phenanthroline test

 

This test was performed based on the method (SZYDŁOWSKA-CZERNIAK et al., 2008) which includes the capacity of the antioxidant to form a complex with 1,10-phenanthroline to reduce Fe³⁺ to Fe²⁺. Briefly, in a microplate, 50 µL of iron chloride (0.2%), then 30 µL of 1,10-phenanthroline and 110 µL of methanol were added to 10 µL of OFSH at different concentrations (from 3.125 to 200 μg/mL). At a wavelength of 510 nm, the absorbance was recorded after leaving the mixture in the incubator at 30°C for 20 minutes. BHT was used as a standard, and the results are presented in A_0.5 values (µg/mL).

 

The permanganate reducing antioxidant capacity

 

The antioxidant activity of OFSH was measured using the PRAC test as published (EFTIMOVÁ et al., 2018). Briefly, 10 µl of OFSH at various concentrations was placed in a microplate. Then, 130 µL of potassium permanganate (KMnO₄) solution and 60 µL of sulfuric acid (H₂SO₄) were added. After incubating the mixture for 5 minutes, the absorbance at 535 nm was measured. BHT was used as a positive reference. The results are presented as a proportion decrease in potassium permanganate. The results are presented as A_0.5 values (µg/mL).

 

Antimicrobial activity

 

The antimicrobial activity of the organic fraction from S. hispanica seeds was evaluated using the disc diffusion method (PEREZ et al., 1990) against eight pathogenic bacteria Escherichia coli (ATCC 25922), Klebsiella pneumonia (ATCC 13883), Vibrio cholera (ATCC 14035), Staphylococcus aureus (ATCC 25923), Listeria monocytogenes (ATCC 35152), Bacillus cereus (ATCC 14579), Salmonella typhimurium (ATCC 14028), Pseudomonas aeruginosa (ATCC 27853) and one pathogenic yeast: Candida albicans (ATCC 10231).

Two different media were used in this part, Muller-Hinton (MH) agar (Biokar Diagnostics, REF 048HA; for the bacterial activity) and Sabouraud agar (Biokar Diagnostics, REF BK027HA; for the antifungal activity against “C. albicans”. The media were poured into sterile Petri dishes and after solidification their surfaces were inoculated with the corresponding microbial suspensions using sterile swabs (at 0.5 McFarland). Next, sterile 6 mm discs (Whatman filter paper) soaked with the extract (dissolved in 2.5% DMSO (at 100 mg/mL) and sterilized through 0.45 µm microfilters) were placed on the surface of the inoculated media.

Disks impregnated with Gentamicin (against bacteria) and amphotericin B (against C. albicans) were used as a positive reference. The plates were then incubated at 37°C for 24 h. After the incubation, the antimicrobial activity was assessed by measuring the diameters of the inhibition zones around each disc. Three replicate plates were inoculated with the same microbial suspension and the whole experiment was repeated thrice (independent repetitions).

 

The α-amylase inhibition activity

 

This experiment aimed to demonstrate the ability of organic fraction from S. hispanica seeds to inhibit α-amylase based on the proposed procedure (ZENGIN et al., 2014). Briefly, 50 μL of α-amylase solution prepared in PBS (pH 6.9) was combined with 25 μL of diluted fraction at different concentrations (from 6.25 to 400 μg/mL). After 10 minutes of incubation at 37°C, 50 µl of 0.1% soluble starch was added to the mixture, and the reaction was incubated for an additional 20 minutes at 37°C. Then, 25 µl of 1M HCl solution was added, followed by 100 µl of iodine/potassium iodine (IKI). At 630 nm, the absorbance was read, and the inhibition percentage of the alpha-amylase enzyme was calculated based on the formula (4) below:

(4) I% = 1 − [(Absc − Abse) − (Abss − Absb)/(Absc − Abse)], where:

Absc: Absorbance [starch+ IKI+ HCL+ Volume of studied fraction+ Volume buffer enzyme];

Abse: Absorbance [starch+ IKI+ HCL+ enzyme];

Abss: Absorbance [starch+ IKI+ HCL+ Volume of studied fraction+ enzyme];

Absb: Absorbance [IKI+ Buffer solution+ Volume of studied fraction].

Chemical analyses

 

The Hewlett-Packard computerized system was used to examine the organic fraction of Chia. This system included a 6890-GC connected to a 5973A MSD and a 30 m × 0.25 mm ID HP-5MS capillary column with a film thickness of 0.25 μm. With an injection volume of 1 μL and an injection temperature of 250°C in split less mode, helium was used as the carrier gas, moving forward at a rate of 0.5 mL/min. Starting at 50°C and maintained for 5 minutes, the oven temperature was programmed to rise to 300°C at a rate of 15°C /min, which was held for 10 minutes. The ionization potential of 70 V, scanning time, and mass range were 2.83 s and 55-550 m/z, respectively. The organic fraction components were identified by comparing mass spectral fragmentation patterns with those stored in the NIST 2020 MS database, Wiley 07 libraries and mass spectra reported in the literature. The concentration of each compound was represented as a percentage (content) and calculated from the corresponding chromatographic peak areas using ChemStation software.

 

Results and discussion

 

Chemical composition of the organic fraction

 

The results of the analysis and identification of components of the organic fraction of S. hispanica obtained using GC-MS are presented in Table 1. Twenty-five bioactive compounds were identified, which constitute an average of 90.40% of the total organic fraction. The chemical composition of OFSH revealed that fatty acids were the main component by 78.93%, followed by steroids (6.95%) and tocopherol (1.87%). Among the fatty acids, omega-6 linoleic acid was the dominant compound, accounting for 57.43%, followed by palmitic acid (8.44%), α-glyceryl linoleate (7.26%), ethyl linoleate (3.35%), and methyl linoleate (1.57%). Our findings are consistent with various studies that suggest that the primary components of S. hispanica organic fraction are polyunsaturated fatty acids. For instance, one research revealed that the oil extracted by different solvents contained linoleic acid alpha and linolenic acid (SILVA et al., 2016). In another study conducted by Tolentino et al. (2014), on the fatty acid content of Chia seeds grown in four states in Mexico, chemical analysis revealed nine fatty acids in Chia oil samples, including alpha-acid, omega-6 acid, and palmitic acid. The percentage of linoleic acid reached 20.57% (GHAFOOR et al., 2020).

 

Table 1 – Chemical components of the organic fraction of S. hispanica seeds

N°	RTa	Componentsb	%c
1	7.44	n-Butylbenzène	0.04
2	7.92	1-Methyl-2-n-propylbenzene	0.09
3	8.00	n-Undécane	0.05
4	8.40	β-Ethylstyrene	0.14
5	10.32	p-Ethylguaiacol	0.20
6	11.12	n-Heptylbenzene	0.06
7	11.2	p-Propylguaiacol	0.13
8	11.37	n-Tetradec-1-ene	0.05
9	11.44	3-Methylindole (Skatol)	0.16
10	11.96	(Z)-Isoeugenol	0.16
11	12.06	n-Octylbenzene	0.08
12	12.31	1-Pentadecene	0.15
13	12.88	Pentadecane	0.21
14	15.32	Palmitonitrile	1.13
15	15.48	Methyl palmitate	0.88
16	15.85	Palmitic acid	8.44
17	16.50	Methyl linoleate	1.57
18	17.15	Linoleic acid	57.43
19	18.22	Ethyl linoleate	3.35
20	19.90	α-Glyceryllinoleate	7.26
21	21.61	β-Tocophérol	1.87
22	21.92	Stigmasta-3,5-diene	3.04
23	22.01	16,17-Didehydropregnenolone acetate	0.65
24	22.96	Methyl glycocholate	0.36
25	23.38	β-Sitostérol	2.90
		Total identified (%)	90.40
		Grouped components
		Fatty acid derivatives	78.93
		Steroids	6.95
		Tocopherol	1.87
		Hydrocarbon derivatives	0.46
		Others	2.19

^a Retention times (RT); ^b Components are listed according to their elution from a HP-5MS column; ^c Relative peak area percentage.

 

Antioxidant properties

 

Seven distinct tests were used to understand the antioxidant effect of the organic fraction of S. hispanica that was extracted using hydro distillation. These tests included the DPPH, ABTS, phenantroline, PRAC, FRAP, CUPRAC and alkaline-DMSO. In Table 2, the data are presented in the form of IC₅₀ and A_0.5 values, and the results were compared with those of butylhydroxytoluene (BHT) and ascorbic acid as positive controls. DPPH (2,2-Diphenyl-1-picrylhydrazyl) is a stable free radical frequently used to test the ability of compounds to become a stable diamagnetic molecule by taking an electron or hydrogen radical (BOUCHOUKH et al., 2019). The OFSH showed good antioxidant activity, with an IC₅₀ value = 71.36 ± 2.93 µg/mL, comparable to BHT with an IC₅₀ value of less than 12.5 µg/mL.

Several studies have used the DPPH assay to estimate the antioxidant activity of S. hispanica. According to the report (SCAPIN et al., 2016), who examined the antioxidant effect of the ethanolic extract of S. hispanica purchased from commercial establishments in Brazil, in January 2013 and the IC₅₀ value obtained was 3.841 mg/mL. In a study (TUNÇİL & ÇELİK, 2019) to compare the compositional properties of white and black Chia seeds commercially available in Turkey, reported an excellent IC₅₀ values for white and black Chia extract (IC₅₀: 1.735 mg/mL and 2.001 mg/mL), respectively. A recent investigation (ABOU ZEID et al., 2022) reported high DPPH scavenging percentage of ethyl acetate extract from aerial parts of S. hispanica with IC₅₀ = 13.11 μg/mL.

Regarding the ABTS test, the OFSH displayed the best activity (IC₅₀ = 14.7 ± 1.7μg/mL). This activity was similar to that of BHT, which exhibited an IC₅₀ value less than 12.5 μg/mL. This result is similar to the IC₅₀ value obtained for black Chia seed ethanol extract (IC₅₀ = 18.11μg/mL) (BANU et al., 2021). However, our sample showed more significant ABTS radical scavenging activity compared to the findings published in previous studies on salvia species (KATANIĆ STANKOVIĆ et al., 2020; MOKHTAR et al., 2023).

The analyzed data in Table 2 for the superoxide radical scavenging test using the alkaline DMSO assay demonstrated that the OFSH seeds exhibited the best activity, with an IC₅₀ value of less than 12.5 μg/mL which is higher than the activity of BHT (IC₅₀ = 40.21 ± 0.3μg/mL). The present results of our study are consistent with the findings (BANU et al., 2021), who reported an IC₅₀ value equal to 14.10 μg/mL. The ability of different Salvia species to scavenge the superoxide (O₂ •-) anion radical has also been the subject of investigations conducted similarly and published (MAMACHE et al., 2020).

 

Table 2 – Antioxidants activity of the organic fraction of S. hispanica seeds

Samples	OFSH	BHT	Ascrobic acid
DPPH IC50(μg/mL)	71.36 ± 2.93	< 12.5	–
ABTS IC50 (μg/mL)	14.9 ± 1.7	<12.5	–
PHE A0.5 (μg/mL)	17.2±2.8	9.71±0.9	–
FRAP A0.5 (μg/mL)	39.3±3.5	–	6.52±0.07
Alkaline-DMSO IC50 (μg/mL	<12.5	40.21±0.3	–
CUPRAC A0.5 (μg/mL)	360.74± 8.6	–	123.02±1.6
PRAC A0.5 (μg/mL)	189.0 ± 0.9	<3.125	–

 

Based on the evaluation of the reduction of metallic iron by the phenanthroline test, it was shown that the OFSH showed a significant reducing capacity (A_0.5 = 17.2 ± 2.8 μg/mL) which is very close to the BHT (A_0.5 = 9.71 ± 0.9 μg/mL). These findings are consistent with the study (MAMACHE et al., 2020) for methanolic extracts of S. verbenaca and S. aegyptiaca obtained from aerial parts (A_0.5 = 18.71 ± 1.03 and 27.03 ± 1.54 μg/mL, respectively).

The reductive ability of organic fraction of S. hispanica seeds depends on reducing ferric ions to the ferrous form in the presence of a reducing agent (an antioxidant). OFSH exhibited a significant reduction potential (A_0.5 = 39.3 ± 3.5 μg/mL) compared with standard ascorbic acid (A_0.5 = 6.52 ± 0.07 μg/mL). The current findings for the studied fraction agreed with the activity value previously reported for ethyl acetate extract from S. hispanica seeds (DIB et al., 2021). The results of our FRAP investigations are better than those reported in a similar study on other Sage species, such as S. nutans, S. nemorasa and S. austriaca (A_0.5= 52.08 ± 0.01; 55.61 ± 0.3 and 80.02 ± 0.05 μg/mL, respectively) (LUCA et al., 2023).

For the permanganate-reducing antioxidant capacity (PRAC) assay, which is based on the reduction of Mn(VII) to Mn(II), the OFSH showed low antioxidant activity (IC₅₀ = 189.0 ± 0.9 μg/mL) compared to BHT < 3.125. The chemiluminescence detection of permanganate is a suitable method to evaluate the antioxidant activity of various beverages, including fruit juices, teas, and other drinks (POPOVIĆ et al., 2012). However, this test has not been examined with salvia species.

On the other hand, the CUPRAC (Cupric ion reducing antioxidant capacity) test involves a reduction in the presence of antioxidants, as indicated by the change from a stable copper (II) – neocuproine complex (blue color) to a stable copper (I) – neocuproine complex (orange color). In this test, the OFSH exhibited low activity (A_0.5 = 360.74 ± 8.68 μg/mL) compared to BHT (A_0.5 = 123.02 ± 1.6 μg/mL). Salvia species showed comparable findings (CHOUIT et al., 2021; MOKHTAR et al., 2023).

 

Antimicrobial activity

 

Using the disc diffusion method, the antimicrobial properties of the organic fraction of S. hispanica seeds dissolved in DMSO were examined against Gram-positive, Gram-negative bacteria and a pathogenic yeast: C. albicans. The results of this evaluation are shown in Table 3. OFSH demonstrated good antagonistic effect against Salmonella, L. monocytogenes and B. cereus, where diameters of the zone of inhibition ranged from 10.33 mm to 12.67 mm. However, OFSH showed no antagonistic effect against S. aureus, E. coli, K. pneumoniae, V. cholerae, P. aeruginosa, and C. albicans. Salmonella was the most susceptible bacterium to OFSH (inhibition zone of 12.67 mm). It should be noted that these results were obtained using a concentration of 100 mg/mL of OFSH. Our findings are in keeping with previous studies. For instance, Elshafie et al. (2018), studied the antimicrobial effect of the essential oil of the aerial parts of S. hispanica against some of phytopathogenic fungi and bacteria. The study showed that the essential oil of Chia significantly reduced the growth of C. michiganensis, B. megaterium, P. savastanoi, B. mojavensis, X. vesicatoria, X. campestris and P. syringae pv. phaseolicola.

In addition, Banu et al. (2021) reported the antibacterial effect of the ethanol fraction of Chia seeds against S. aureus, E. coli, M. luteus, B. subtilis and S. flexneri. Among these, S. aureus was the most susceptible bacterium, with a zone of inhibition of 31 mm at a concentration of 500 μg/mL. Mokhtar et al. (2023) showed the antibacterial effect of the Chia leaves extracts against Gram-positive bacteria, including E. faecalis, M. luteus, S. aureus, and S. epidermidis.

 

Table 3 – Antimicrobial activity of organic fraction of S. hispanica seeds

Strains	Inhibition zone (mm)	Positive control
E. coli	6.67 ± 0.5	22.33 ± 0.5
K. pneumoniae	6.17 ± 0.2	28.67 ± 1.5
V. cholerae	6.17 ± 0.2	36.67 ± 0.5
S. aureus	7.17±0.2	36.33 ± 0.5
L. monocytogenes	12 ± 1	26.67 ± 05
B. cereus	10.33 ± 0.5	34.67 ± 0.5
S. typhimurium	12.67 ± 0.5	33.67 ± 1.1
P. aeruginosa	6.17 ± 0.2	26.67 ± 0.5
C. albicans	6.17 ± 0.2	19.33 ± 0.5

 

On the other hand, our findings showed that OFSH was able to inhibit the growth of two Gram-positive (L. monocytogenes and B. cereus) and one Gram-negative (S. typhimurium).

These bacteria are known to be responsible for some food poisoning and can develop new antibio-resistance to some antibiotics, which allows us to say that our OFSH can constitute a good alternative to antibiotics.

 

In vitro enzyme inhibitory activity

 

Enzyme inhibition is one of the most intriguing and extensively researched therapeutic strategies for the pharmaceutical and cosmetic sectors. These drugs are utilized in clinical settings to treat a variety of illnesses, including diabetes, obesity, and Alzheimer’s disease (ÖKTEN et al., 2019).

It has been found that synthetic inhibitors can cause adverse effects such as gastrointestinal problems and liver toxicity. However, there is great interest in discovering natural inhibitors without side effects compared to synthetic inhibitors (GONÇALVES & ROMANO, 2017; RODRIGUES et al., 2018). OFSH showed the highest α-amylase inhibitory activity (IC₅₀ = 34.97 ± 0.68 μg/mL) compared to the reference Acarbose enzyme (IC₅₀ = 6.96 ± 0.4 μg/mL) (Figure 1). A recent study (ABDEL GHANI et al., 2023) to evaluate the anti-diabetic effect of dichloromethane extract from the aerial parts revealed biological results (IC₅₀ = 673.25 μg/mL) (BANU et al., 2021), found that the inhibitory effect of Chia seeds was IC₅₀ = 121.46 μg/mL. However, the enzyme inhibitory activity assay results in our studies are better compared to many chemical studies that have been reported on Salvia species; for example, a study reported an inhibitory effect on α-amylase of methanolic fractions of S. officinalis, S. macilenta, S. mirzayanii and S. santolinifola (IC₅₀ = 54.9 ± 5.7; 103.7 ± 1.1; 114.8 ± 11.1 and 54.7 ± 9.6ug/mL) (JAVID et al., 2022), S. aegyptiaca and S. verbenaca (IC₅₀= 86.12 ± 0.08 and 101.30 ± 0.08 μg/mL), respectively (MAMACHE et al., 2020).

In this study, the organic fraction from Chia seeds showed higher antioxidant, antidiabetic, and antibacterial activities, which can be attributed to the richness of bioactive compounds. These compounds include fatty acids, steroids, and tocopherols. The organic fraction contained 78.92% fatty acid derivatives (such as methyl palmitate, palmitic acid, methyl linoleate, linoleic acid, ethyl linoleate, and α-glyceryl linoleate), 6.95% steroids (including stigmasta-3,5-diene, 16,17 didehydropregnenolone acetate, methyl glycocholate, and β-sitosterol), and 1.87% tocopherols. Fatty acids (FAs) play essential roles in preventing many diseases and abnormal differentiation problems. A recent study reported the importance of fatty acids in fighting cardiovascular diseases, inflammatory reactions, and their antioxidant activities (GAWRON-SKARBEK et al., 2023). Linoleic acid, or omega 6 (LA), is one of the polyunsaturated fatty acids (PUFA) that plays a crucial role in the human body and works to reduce triglyceride levels, thus protecting against the risks of heart disease, strokes, and cancer. It is found in many foods, such as nuts, seeds, and vegetable oils. The percentage of linoleic acid in the extracted sample was 57.43%. These data indicate that linoleic acid (LA) would protect against free radicals according to the study (HENRY et al., 2002), which reported that several essential fatty acids FAs including (linolenic acid, linoleic acid, palmitic acid, oleic acid, and lauric acid ) can act as antioxidants or pro-oxidants (LALITHADEVI et al., 2018) reported that conjugated linoleic acid (CLA) has potential health benefits such as antioxidant properties, weight loss, and anti-aging. LA has been shown to inhibit the growth of colorectal cancer cells by enhancing the cellular redox state and promoting the prevention of type 2 diabetes (LU et al., 2010; ZONG et al., 2019). Another study, (YOON et al., 2021), reported that omega 6 contains a multi-targeted inhibitor of non-receptor type protein tyrosine phosphatase (types 1, 9, and 11) and has antidiabetic activity (T2DM). FAs displayed antibacterial activity against some strains (S. aureus and B. subtilis). Stigmata 3,5-diene is a well-known plant sterol that has gained popularity in traditional medicine due to its various biological properties, including antioxidant, anti-inflammatory, antibacterial, antiviral, antidiabetic, antifungal, anti-immune, antiparasitic, and neuroprotective properties (KUSUMAH et al., 2020).

 

Figure 1 – IC₅₀ values of α-amylase inhibitory activity of the organic fraction of Chia seeds.

 

One report indicated that Sigmasta 3,5-diene has significant anti-inflammatory effects and can exert antidiabetic properties by lowering fasting glucose and blood insulin levels (BAKRIM et al., 2022). The β-sitosterol derivative showed antimicrobial activity against Salmonella typhimurium, Staphylococcus aureus, Klebsiella pneumoniae, Escherichia coli, Proteus mirabilis and Bacillus subtilis (NJINGA et al., 2016). The results of one study revealed that β-sitosterol in 1,2-dimethylhydrazine caused an augmentation of enzymatic and non-enzymatic antioxidants in mice, and this compound has been recommended as an effective drug for colorectal cancer (BASKAR et al., 2012). Vitamin β-Tocopherol is essential as an antioxidant and anti-inflammatory (RIZVI et al., 2014).

 

Conclusion

 

Recently, there has been an increasing demand for natural additives instead of synthetic preservatives. As a result, academic research on the antioxidant and antibacterial properties of extracts, essential oils, and fixed oils from various plant species has also increased. In this context, studying the organic fraction of distilled Salvia hispanica seeds (OFSH) may be of great interest. Chia is rich in bioactive compounds, such as fatty acid derivatives, steroids, and tocopherol, which showed high antioxidant, antidiabetic, and antibacterial activities. Our data show that S. hispanica could be an excellent alternative source for therapeutic medicine, especially for the treatment of chronic diseases such as diabetes, coronary heart disease, cancer and fungal infections.

 

Conflicts of interest

 

The author declares no conflicts of interest regarding the work presented here.

 

Authors’ contribution

 

Ibtissem Rahmoune – methodology, data curation, writhing original draft; Samira Karoune – validation, reviewing and ressources; Madani Sarri – wrote the paper; Clara Azzam – review; Somia Saad – methodology, conceptualization, review, validation; Abdelhamid Foughalia – antimicrobial activity; Farid Chebrouk – GC/MS analysis; Hana Abidat – experimental assays; Mohamed Seif Allah Kechebar – review.

 

Disclosure statement

 

This work was financed by ERANET FOSC under the title of Integrated Chia and Oyster Mushroom System for a Sustainable Food Value Chain in Africa (CHIAM), supported by the General Directorate of Scientific Research and Technological Development, Algeria.

 

References

 

ABDEL GHANI, A. E.; AL-SALEEM, M. S. M.; ABDEL-MAGEED, W. M.; ABOUZEID, E. M.; MAHMOUD, M. Y.; ABDALLAH, R. H. UPLC-ESI-MS/MS Profiling and cytotoxic, antioxidant, anti-Inflammatory, antidiabetic, and antiobesity activities of the non-polar fractions of Salvia hispanica L. aerial parts. Plants, v. 12, n. 5, p. 1-2, 2023. https://doi.org/10.3390/plants12051062

ABOU ZEID, E. M.; ABDEL GHANI, A. E.; MAHMOUD, M. Y.; ABDALLAH, R. H. Phytochemical investigation and biological screening of ethyl acetate fraction of Salvia hispanica L. aerial parts. Pharmacognosy Journal, v. 14, n. 1, p. 226-234, 2022. https://doi.org/10.5530/pj.2022.14.28

APAK, R.; GÜÇLÜ, K.; ÖZYÜREK, M.; KARADEMIR, S. E. Novel total antioxidant capacity index for dietary polyphenols and vitamins C and E, using their cupric ion reducing capability in the presence of neocuproine: CUPRAC method. Journal of Agricultural and Food Chemistry, v. 52, n. 26, p. 7970-7981, 2004. https://doi.org/10.1021/jf048741x

BAKRIM, S.; BENKHAIRA, N.; BOURAIS, I.; BENALI, T.; LEE, L. H.; EL OMARI, N.; SHEIKH, R. A.; GOH, K. W.; MING, L. C.; BOUYAHYA, A. Health benefits and pharmacological properties of stigmasterol. Antioxidants, v. 11, n. 10, p. 1-32, 2022. https://doi.org/10.3390/antiox11101912

BANU, S. A.; JOHN, S.; MONICA, S. J.; SARASWATHI, K.; ARUMUGAM, P. Screening of secondary metabolites, bioactive compounds, in vitro antioxidant, antibacterial, antidiabetic and anti-inflammatory activities of Chia seeds (Salvia hispanica). Research Journal of Pharmacy and Technology, v. 12, n. 14, p. 6289-6294, 2021. https://doi.org/10.52711/0974-360X.2021.01088

BASKAR, A. A.; AL NUMAIR, K. S.; GABRIEL PAULRAJ, M.; ALSAIF, M. A.; MUAMAR, M. AL.; IGNACIMUTHU, S. β-sitosterol prevents lipid peroxidation and improves antioxidant status and histoarchitecture in rats with 1,2-dimethylhydrazine-induced colon cancer. Journal of Medicinal Food, v. 15, n. 4, p. 335-343, 2012. https://doi.org/10.1089/jmf.2011.1780

BOUCHOUKH, I.; HAZMOUNE, T.; BOUDELAA, M.; BENSOUICI, C.; ZELLAGUI, A. Anticholinesterase and antioxidant activities of foliar extract from a tropical species: Psidium guajava L. (Myrtaceae) grown in Algeria. Pharmacy and Medical Sciences, v. 32, n. 3, p. 160-167, 2019. https://doi.org/10.2478/cipms-2019-0029

CAHILL, J. P. Ethnobotany of Chia, Salvia hispanica. Economic Botany, v. 57, n. 4, p. 604-618, 2003. https://www.jstor.org/stable/4256743

CHOUIT, H.; TOUAFEK, O.; BRADA, M.; BENSSOUICI, C.; FAUCONNIER, M. L.; EL HATTAB, M. GC-MS analysis and biological activities of Algerian Salvia microphylla essential oils. Journal of the Mexican Chemical Society, v. 65, n. 4, p. 582-601, 2021. https://doi.org/10.29356/JMCS.V65I4.1581

DIB, H.; SELADJI, M.; BENCHEIKH, F. Z.; FARADJI, M.; BENAMMAR, C.; BELARBI, M. Phytochemical screening and antioxidant activity of Salvia hispanica. Journal of Pharmaceutical Research International, v. 33, n. 41, p.167-174, 2021. https://doi.org/10.9734/jpri/2021/v33i41a32314

EFTIMOVÁ, Z.; EFTIMOVÁ, J.; BALÁŽOVÁ, L. Antioxidant activity of Tokaj essence. Potravinarstvo Slovak Journal of Food Sciences, v. 12, n. 1, p. 323-329, 2018. https://doi.org/10.5219/829

ELSHAFIE, H. S.; ALIBERTI, L.; AMATO, M.; DE FEO, V.; CAMELE, I. Chemical composition and antimicrobial activity of Chia (Salvia hispanica L.) essential oil. European Food Research and Technology, v. 244, n. 9, p. 1675-1682, 2018. https://doi.org/10.1007/s00217-018-3080-x

FOLLI, F.; CORRADI, D.; FANTI, P.; DAVALLI, A.; PAEZ, A.; GIACCARI, A.; PEREGO, C.; MUSCOGIURI, G. The role of oxidative stress in the pathogenesis of type 2 Diabetes Mellitus micro-and macrovascular complications: avenues for a mechanistic-based therapeutic approach. Diabetes Reviews, v. 7, n. 5, p. 313-324, 2011. https://doi.org/10.2174/157339911797415585

GAWRON-SKARBEK, A.; GULIGOWSKA, A.; PRYMONT-PRZYMIŃSKA, A.; NOWAK, D.; KOSTKA, T. The anti-inflammatory and antioxidant impact of dietary fatty acids in cardiovascular protection in older adults may be related to vitamin C intake. Antioxidants, v. 12, n. 2, p. 1-12, 2023. https://doi.org/10.3390/antiox12020267

GHAFOOR, K.; AHMED, I. A. M.; ÖZCAN, M. M.; AL-JUHAIMI, F. Y.; BABIKER, E. E.; AZMI, I. U. An evaluation of bioactive compounds, fatty acid composition and oil quality of Chia (Salvia hispanica L.) seed roasted at different temperatures. Food Chemistry, v. 333, n. 5, p. 1-7, 2020. https://doi.org/10.1016/j.foodchem.2020.127531

GONÇALVES, S.; ROMANO, A. Inhibitory properties of phenolic compounds against enzymes linked with human diseases. In: SOTO-HERNANDEZ, M.; PALMA-TENANGO, M.; GARCIA-MATEOS, M. R. (Eds.). Phenolic compounds – biological activity. InTech Open, p. 1-20, 2017. https://doi.org/10.5772/66844

GRANCIERI, M.; MARTINO, H. S. D.; GONZALEZ DE MEJIA, E. Chia Seed (Salvia hispanica L.) as a source of proteins and bioactive peptides with health benefits: a review. Comprehensive Reviews in Food Science and Food Safety, v. 18, n. 2, p. 480-499, 2019. https://doi.org/10.1111/1541-4337.12423

HENRY, G. E.; MOMIN, R. A.; NAIR, M. G.; DEWITT, D. L. Antioxidant and cyclooxygenase activities of fatty acids found in food. Journal of Agricultural and Food Chemistry, v. 50, n. 8, p. 2231-2234, 2002. https://doi.org/10.1021/jf0114381

ISHAK, I.; HUSSAIN, N.; COOREY, R.; GHANI, M. A. Optimization and characterization of Chia seed (Salvia hispanica) oil extraction using supercritical carbon dioxide. Journal of CO₂ Utilization, v. 4, n. 5, p. 1-14, 2021. https://doi.org/10.1016/j.jcou.2020.101430

JAVID, H.; MOEIN, S.; MOEIN, M. An investigationof the inhibitory effects of dichloromethane and methanol extracts of Salvia macilenta, Salvia officinalis, Salvia santolinifola and Salvia mirzayanii on diabetes marker enzymes, an approach for the treatment diabetes. Clinical Phytoscience, v. 8, n. 1, p. 1-8, 2022. https://doi.org/10.1186/s40816-022-00339-y

KATANIĆ STANKOVIĆ, J. S.; SREĆKOVIĆ, N.; MIŠIĆ, D.; GAŠIĆ, U.; IMBIMBO, P.; MONTI, MIHAILOVIĆ, V. Bioactivity, biocompatibility and phytochemical assessment of lilac sage, Salvia verticillata L. (Lamiaceae) – a plant rich in rosmarinic acid. Industrial Crops and Products, v. 143, p. 1-11, 2020. https://doi.org/10.1016/j.indcrop.2019.111932

KOEPKE, J. I.; WOOD, C. S.; TERLECKY, L. J.; WALTON, P. A.; TERLECKY, S. R. Progeric effects of catalase inactivation in human cells. Toxicology and Applied Pharmacology, v. 232, n. 1, p. 99-108, 2008. https://doi.org/10.1016/j.taap.2008.06.004

KUNCHANDY, E.; RAO, M. N. A. Oxygen radical scavenging activity of Curcumin. International Journal of Pharmaceutics, v. 58, n. 3, p. 237-240, 1990. https://doi.org/10.1016/0378-5173(90)90201-E

KUSUMAH, D.; WAKUI, M.; MURAKAMI, M.; XIE, X.; YUKIHITO, K.; MAEDA, I. Linoleic acid, α-linolenic acid, and monolinolenins as antibacterial substances in the heat-processed soybean fermented with Rhizopus oligosporus. Bioscience, Biotechnology and Biochemistry, v. 84, n. 6, p. 1285-1290, 2020. https://doi.org/10.1080/09168451.2020.1731299

LALITHADEVI, B.; MUTHIAH, N. S.; MURTY, K. S. N. Antioxidant activity of conjugated linoleic acid. Asian Journal of Pharmaceutical and Clinical Research, v. 11, n. 11, p. 169-173, 2018. https://doi.org/10.22159/ajpcr.2018.v11i11.27700

LIN, K.Y.; DANIEL, J. R.; WHISTLER, R. L. Structure of chia seed polysaccharide exudate. Carbohydrate Polymers, v. 23, n. 1, p. 1-6, 1994. https://doi.org/10.1016/0144-8617(94)90085-X

LU, X.; YU, H.; MA, Q.; SHEN, S.; DAS, U. N. Linoleic acid suppresses colorectal cancer cell growth by inducing oxidant stress and mitochondrial dysfunction. Lipids in Health and Disease, v. 9, n. 106, p. 1-11, 2010. http://www.lipidworld.com/content/9/1/106

LUCA, S. V.; SKALICKA-WOŹNIAK, K.; MIHAI, C. T.; GRADINARU, A. C.; MANDICI, A.; CIOCARLAN, N.; MIRON, A.; APROTOSOAIE, A. C. Chemical profile and bioactivity evaluation of Salvia species from Eastern Europe. Antioxidants, v. 12, n. 8, p. 1-21, 2023. https://doi.org/10.3390/antiox12081514

MAMACHE, W.; AMIRA, S.; BEN SOUICI, C.; LAOUER, H.; BENCHIKH, F. In vitro antioxidant, anticholinesterases, anti-α-amylase, and anti-α-glucosidase effects of Algerian Salvia aegyptiaca and Salvia verbenaca. Journal of Food Biochemistry, v. 44, n. 11, p. 1-15, 2020. https://doi.org/10.1111/jfbc.13472

MARTÍNEZ-CRUZ, O.; PAREDES-LÓPEZ, O. Phytochemical profile and nutraceutical potential of Chia seeds (Salvia hispanica L.) by ultra-high performance liquid chromatography. Journal of Chromatography A, v. 1346, p. 43-48, 2014. https://doi.org/10.1016/j.chroma.2014.04.007

MOKHTAR, A.; SOUHILA, T.; NACÉRA, B.; AMINA, B.; ALGHONAIM, M. I.; ÖZTÜRK, M.; ALSALAMAH, S. A.; MIARA, M. D.; BOUFAHJA, F.; BENDIF, H. In vitro antibacterial, antioxidant, anticholinesterase, and antidiabetic activities and chemical composition of Salvia balansae. Molecules, v. 28, n. 23, p. 1-26, 2023. https://doi.org/10.3390/molecules28237801

NJINGA, N. S.; SULE, M. I.; PATEH, U. U.; HASSAN, H. S.; ABDULLAHI, S. T.; ACHE, R. N. Isolation and antimicrobial activity of β-Sitosterol-3-O-Glucoside from Lannea Kerstingii Engl. & K. Krause (Anacardiacea). Journal of Health Science and Allied Sciences, v. 6, n. 1, p. 4-8, 2016. https://doi.org/10.1055/s-0040-1708607

ÖKTEN, S.; EKIZ, M.; KOÇYIĞIT, Ü. M.; TUTAR, A.; ÇELIK, İ.; AKKURT, M.; GÖKALP, F.; TASLIMI, P.; GÜLÇIN, İ. Synthesis, characterization, crystal structures, theoretical calculations and biological evaluations of novel substituted tacrine derivatives as cholinesterase and carbonic anhydrase enzymes inhibitors. Journal of Molecular Structure, v. 11, n. 75, p. 906-915, 2019. https://doi.org/10.1016/j.molstruc.2018.08.063

OLIVOS-LUGO, B. L.; VALDIVIA-LÓPEZ, M. Á.; TECANTE, A. Thermal and physicochemical properties and nutritional value of the protein fraction of Mexican Chia seed (Salvia hispanica L.). Food Science and Technology International, v. 16, n. 1, p. 89-96, 2010. https://doi.org/10.1 177/1082013209353087

OYAIZU, M. Studies on products of browning reaction: antioxidative activities of browning reaction prepared from glucosamine, Japan Journal of Nutrition, v. 44, n. 6, p. 307-315, 1986. https://doi.org/10.5264/eiyogakuzashi.44.307

PEREZ, C.; PAULI, M.; BAZERQUE, P. An antibiotic assay by agar well diffusion method. Acta Biologiae et Medicinae Experimentalis, v. 15, p. 113-115, 1990.

POPOVIĆ, B. M.; ŠTAJNER, D.; SLAVKO, K.; SANDRA, B. Antioxidant capacity of cornelian cherry (Cornus mas L.) – Comparison between permanganate reducing antioxidant capacity and other antioxidant methods. Food Chemistry, v. 134, n. 2, p. 734-741, 2012. https://doi.org/10.1016/j.foodchem.2012.02.170

RE, R.; PELLEGRINI, N.; PROTEGGENTE, A.; PANNALA, A.; YANG, M.; RICE-EVANS, C. Original contribution antioxidant activity applying an improved abts radical cation decolonization assay. Free Radical Biology & Medicine. v. 26, n. 10, p. 1231-1237, 1999. https://doi.org/10.1016/s0891-5849(98)00315-3

RIZVI, S.; RAZA, S. T.; AHMED, F.; AHMAD, A.; ABBAS, S.; MAHDI, F. The role of vitamin E in human health and some diseases. Sultan Qaboos University Medical Journal, v. 14, n. 2, p. 157-165, 2014. https://pubmed.ncbi.nlm.nih.gov/24790736/

RODRIGUES, M. J.; PEREIRA, C. A.; OLIVEIRA, M.; NENG, N. R.; NOGUEIRA, J. M. F.; ZENGIN, G.; MAHOMOODALLY, M. F.; CUSTÓDIO, L. Sea rose (Armeria pungens (Link) Hoffmanns. & Link as a potential source of innovative industrial products for anti-ageing applications. Industrial Crops and Products, v. 12, n. 1, p. 250-257, 2018. https://doi.org/10.1016/j.indcrop.2018.05.018

SANDOVAL-OLIVEROS, M. R.; PAREDES-LÓPEZ, O. Isolation and characterization of proteins from Chia seeds (Salvia hispanica L.). Journal of Agricultural and Food Chemistry, v. 61, n. 1, p. 193-201, 2013. https://doi.org/10.1021/jf3034978

SCAPIN, G.; SCHMIDT, M. M.; PRESTES, R. C.; ROSA, C. S. Phenolics compounds, flavonoids and antioxidant activity of Chia seed extracts (Salvia hispanica) obtained by different extraction conditions. International Food Research Journal, v. 23, n. 6, p. 2341-2346, 2016. http://www.ifrj.upm.edu.my/23%20(06)%202016/(5).pdf

SILVA, C.; GARCIA, V. A. S.; ZANETTE, C. M. Chia (Salvia hispanica L.) oil extraction using different organic solvents oil. International Food Research Journal, v. 23, n. 3, p. 998-1004, 2016. http://www.ifrj.upm.edu.my/23%20(03)%202016/(13).pdf

SZYDŁOWSKA-CZERNIAK, A.; DIANOCZKI, C.; RECSEG, K.; KARLOVITS, G.; SZŁYK, E. Determination of antioxidant capacities of vegetable oils by ferric-ion spectrophotometric methods. Talanta, v. 76, n. 4, p. 899-905, 2008. https://doi.org/10.1016/j.talanta.2008.04.055

TARLING, C. A.; WOODS, K.; ZHANG, R.; BRASTIANOS, H. C.; BRAYER, G. D.; ANDERSEN, R. J.; WITHERS, S. G. The search for novel human pancreatic α-amylase inhibitors: high-throughput screening of terrestrial and marine natural product extracts. ChemBioChem, v. 9, n, 3, p. 433-438, 2008. https://doi.org/10.1002/cbic.200700470

TOLENTINO, R. G.; VEGA, L. R.; VEGA, Y.; LEON, S. V.; FONTECHA, J.; RODRÍGUEZ, L. M.; MEDINA, A. E. Fatty acid content in Chia (Salvia hispanica L.) seeds grown in four Mexican states. Revista Cubana de Plantas Medicinales, v. 19, n. 1, p.199-207, 2014. https://www.medigraphic.com/pdfs/revcubplamed/cpm-2014/cpm143h.pdf

TUNÇİL, Y. E.; ÇELİK, Ö. F. Total phenolic contents, antioxidant and antibacterial activities of Chia seeds (Salvia hispanica L.) having different coat color. Akademik Ziraat Dergisi, v. 8, n. 1, p. 113-120, 2019. https://doi.org/10.29278/azd.593853

YOON, S. Y.; AHN, D.; HWANG, J. Y.; KANG, M. J.; CHUNG, S. J. Linoleic acid exerts antidiabetic effects by inhibiting protein tyrosine phosphatases associated with insulin resistance. Journal of Functional Foods, v. 83, n. 9, p. 1-6, 2021. https://doi.org/10.1016/j.jff.2021.104532

ZENGIN, G.; SARIKURKCU, C.; AKTUMSEK, A.; CEYLAN, R.; CEYLAN, O. A comprehensive study on phytochemical characterization of Haplophyllum myrtifolium Boiss. endemic to Turkey and its inhibitory potential against key enzymes involved in Alzheimer, skin diseases and type II diabetes. Industrial Crops and Products, v. 5, n. 3, p. 244-251, 2014. https://doi.org/10.1016/j.indcrop.2013.12.043

ZONG, G.; LIU, G.; WILLETT, W. C.; WANDERS, A. J.; ALSSEMA, M.; ZOCK, P. L.; HU, F. B.; SUN, Q. Associations between linoleic acid intake and incident type 2 diabetes among U.S. men and women. Diabetes Care, v. 42, n. 8, p. 1406-1413, 2019. https://doi.org/10.2337/dc19-0412

 

 

 

Received on August 17, 2024

Returned for adjustments on October 7, 2024

Received with adjustments on October 8, 2024

Accepted on October 15, 2024