530
Views
5
CrossRef citations to date
0
Altmetric
Original Articles

The effect of genetic variation and nitrogen fertilization on productive characters of Greek oregano

, , , &
Pages 372-379 | Received 25 Nov 2016, Accepted 11 Jan 2017, Published online: 03 Feb 2017

ABSTRACT

This study aims to investigate the response of 10 Greek Oregano (Origanum vulgare subsp. hirtum) populations, collected across Greece, under 3 levels of N-fertilization during 2012 and 2013. The populations were differentiated for dry matter (from 32.7 to 63.3 g·pot−1), for essential oil content (from 2.31 to 5.86 ml·100−1 g dry weight) and for amount of essential oil (from 1.37 to 2.46 ml·pot−1), for both years. Those with the highest dry matter (1-“Palaiochori” and 5-“Gliki”) and the highest essential oil content (10-“Gytheio” and 9-“Achladocastro”) were superior by 30%, as compared to the general mean of the experiment. The populations 3-“Litochoro” and 5-“Gliki” had an increased amount of essential oil (24%) as compared to the general mean of the experiment. An additional nitrogen supply (N0 to N1 level) increased dry matter production and amount of essential oil per pot, while decreased essential oil content for all populations. Further increase of nitrogen supply, favored six populations for dry matter production and two populations for amount of essential oil per pot while had almost no effect on five populations for essential oil content. The superior populations could be used in a breeding program as starting material for the development of new cultivars.

Introduction

Origanum vulgare ssp. hirtum is geographically distributed in Mediterranean-type ecosystems and mountain woodlands. It is the commonest O. vulgare subspecies in Greece (Vokou et al. Citation1993) that is widely used as a spice under the name ‘Greek oregano’ (Kokkini & Vokou Citation1989). ‘Greek oregano’, has the best quality of all similar spices and, therefore, many studies were focused on its geographical distribution and chemical features of their essential oils as collected from natural habitats (Kokkini Citation1997; Skoula & Harborne Citation2002). It is reported that the essential oil content of O. vulgare ssp. hirtum can reach up to 8%, with high percentage of carvacrol that can reach up to 95% and/or thymol (Kokkini & Vokou Citation1989; Kokkini et al. Citation1994; Johnson et al. Citation2004). The essential oil content and their constituents have a great variation within other Origanum species. It is reported that the essential oil content of Origanum onites is ranging from 1.8% to 4.5%, including a carvacrol content ranging from 51.0% to 84.5%; regarding the O. vulgare spp. viridulum the recorded essential oil was ranged from 0.3% to 0.8% having a carvacrol content in a range from 40.0% to 45.1%, while the essential oil of O. vulgare spp. vulgare is ranging from 0.1% to 0.3% including only traces of carvacrol (Kokkini & Vokou Citation1989).

However, the collection of wild aromatic and medicinal species from natural habitats for wide use, before seed set, results in low regeneration and gradual population decline (Abbad et al. Citation2011). Therefore, the cultivation of native species could ensure their conservation and protection in the natural habitats while allowing their sustainable utilization. For this situation, an extensive study of the necessary inputs that can affect the growth and development of medicinal and aromatic plants under cultivation is required (Jamali et al. Citation2014).

In the case of Greek oregano, another important motive for the optimal exploitation of its genetic variability found in Greece is the high commercial value and potential profit derived from its cultivation which can reach up to 2500 euros per hectare (Kintzios Citation2002). Additionally, oregano consumption has increased, not only for its use as a spice, but also because of its therapeutic benefits on human health due to antioxidative, antimicrobial and antifungal properties (Baratta et al. Citation1998; Rhayour et al. Citation2003; Gavaric et al. Citation2015; Adame-Gallegos et al. Citation2016).

Recently, several researchers investigated the factors that might affect the production and quality of oil yield of oregano species under cultivation conditions (Chatzopoulou et al. Citation2004; Kizil et al. Citation2009) or the vegetative propagation methods (Bilalis et al. Citation2012). The optimal combination for nitrogen supply and water availability was studied further for their influence to the production of optimum herbage and essential oil content in an O. vulgare genotype (Said-Al Ahl et al. Citation2009). Initially, the performance of selected populations from different subspecies of O. vulgare was investigated under different nitrogen fertilization levels and soil moisture regimes (Azizi et al. Citation2009). Also, selected populations of the O. vulgare ssp. viridulum were evaluated under cropping conditions, in Southern Italy (De Falco et al. Citation2014). Other field studies were conducted to evaluate the impact of nitrogen availability on oregano plant growth and characteristics (Sotiropoulou & Karamanos Citation2010; Karamanos & Sotiropoulou Citation2013; Dordas Citation2016) or the effect of calcium and magnesium foliar application to the dry matter production and oil yield (Dordas Citation2009). Nitrogen application affected positively the amount of essential oil production per hectare due to the increased vegetative growth, while there was no effect on oil concentration (Sotiropoulou & Karamanos Citation2010). In a recent study, it was found that the use of different organic fertilizers in peppermint affected the amount of essential oil, while having minor effects on the essential oil composition (Costa et al. Citation2013). Apart from cultivation and environmental conditions, oregano essential oil content and composition were significantly affected by genotype which has a major contribution to the observed variability of the above characteristics (Novak et al. Citation2003). More specifically, important variability was observed in the yield and quality of O. vulgare ssp. hirtum, among wild populations widespread in most parts of Greece (Kokkini & Vokou Citation1989; Vokou et al. Citation1993; Kokkini Citation1997; Gavalas et al. Citation2011). Despite the above, there is little available information on the impact of genotype on yield and quality and their interaction with nutrient supplies, since other researchers use only few genotypes (Azizi et al. Citation2009; Dordas Citation2009, Citation2016; Karamanos & Sotiropoulou Citation2013).

The aim of the current study was: (i) to assess the variation of yield and oil content among 10 Greek oregano (O. vulgare ssp. hirtum) populations originated from diverse geographical areas across Greece and (ii) to evaluate the response of these populations to nitrogen fertilization.

Materials and methods

Experimental set-up

The experiment was conducted in a greenhouse located at Omolio, Larissa (39°53'N, 22°38'E) during the years 2012 and 2013. Seeds of oregano (O. vulgare ssp. hirtum) were collected from 10 regions of Greece with diverse agro-climatic conditions ( and ). The collected seeds were sown in a nursery and the most vigorous uniform plants were transplanted in 7.5 l plastic pots (No. 200–23.5 × 22 cm) (five plants per pot). The soil used as substrate, was collected from a field in Omolio at a depth of 0–20 cm and had the following characteristics: loam (55% sand, 14% silt and 31% clay), pH 7.8 (1:1 H2O), Ν 10.5 (μg·g−1), P 15.7 (Olsen μg·g−1), K+ 150 (exchangeable μg·g−1), Ca+2 740 (exchangeable g·Kg−1), Mg+2 105 (exchangeable μg·g−1) and 1.9% organic matter. Irrigation corresponded to 80% of the water holding capacity of the pots and was maintained stable during plant growth.

Figure 1. Collection sites of Greek oregano plants in relation to the distinct floristic regions of Greece, as they are designated in Flora Hellenica (adapted from Strid & Tan Citation2002).

Figure 1. Collection sites of Greek oregano plants in relation to the distinct floristic regions of Greece, as they are designated in Flora Hellenica (adapted from Strid & Tan Citation2002).

Table 1. The geographic location and the climatic characteristics (temperature and precipitation) of the collection sites of Greek oregano populations for the annual and the cultivation period (March–July) (average of the period 2010–2015).

Three nitrogen nutrition levels were applied: N0 (control, without fertilization), N1 (0.6 N g·pot−1) and N2 (1.2 N g·pot−1). Ammonium nitrate (NH4NO3) was dissolved in water and applied to each pot in the middle of April. A dish was placed under each pot to prevent nutrient leaching, and the collected leachate in the dish was applied back to each pot before watering. Two harvests were carried out at the end of each growing cycle in 2012 and 2013. To determine dry matter production, plants were cut at 5 cm above soil level and dried in an air-circulating oven at 40°C for 4 days. Essential oils were isolated by hydro-distillation for 3 h using a Clevenger apparatus according to Europaean Pharmacopeia (EDQM Citation2005) and the essential oil content was expressed in ml 100−1 g dry weight (DW).

Statistics

Homogeneity of variances was checked for all measurements and derived data, before the analysis of variance (ANOVA). A completely randomized experimental design was conducted as a two factorial pot experiment with three replications. The 1rst factor was the nitrogen supply level with three treatments [N0 (control, without fertilization), N1 (0.6 N g·pot−1) and N2 (1.2 N g·pot−1)] and the 2nd factor was the genotype expressed thought the 10 populations of O. vulgare ssp. hirtum, as described above. The experiment included 90 pots in total (3 nitrogen levels × 10 populations × 3 replications), while each pot contained 5 plants. Tukey’s test (P = .05) was used to find significant differences among the means. All statistical analyses were performed using the SPSS software package (ver. 18, SPSS Inc., Chicago, USA).

Results

Effects of nitrogen supply on dry matter production, and essential oil content and yield

The studied parameters were differentiated under the different nitrogen fertilization levels (). Increased nitrogen availability during plant growth has resulted in higher dry matter accumulation, up to level N1 for both years of the experimentation, by an average of 24.0% as compared to the N0 (). Also, it was found that N1 level was sufficient for the achievement of the highest dry matter production for both years, since there was no significant differences with the level N2 ().

Table 2. Over year ANOVA of Greek oregano populations and nitrogen supply levels for dry matter (g·pot−1), essential oil content (ml·100−1 g DW) and amount of essential oil per pot (ml·pot−1) and their interactions.

Table 3. Dry matter (g·pot−1), essential oil content (ml 100−1 g DW) and amount of essential oil per pot (ml·pot−1) of the three nitrogen levels (N0, N1 and N2), in 2012, in 2013 and in over year analysis of Greek oregano populations.

On the contrary, it was observed that increased nitrogen availability resulted in reduced essential oil content, with the lowest value found at the N2 level, lower on average by 11.8% compared to N0 (4.15 vs. 4.71 ml 100−1 g DW, respectively) ().

Finally, the total amount of essential oil per pot, which was estimated by multiplying the dry matter and essential oil content, was affected positively by nitrogen supply; the highest value was recorded at level N1, which was increased by 12.4% compared to level N0, producing 2.06 ml·pot−1. The additional nitrogen supply at the N2 level did not contribute to a further production of essential oil since no significant difference was detected (). The impact of nitrogen fertilization was similar for both years for all recorded variables, since no Y × N interactions were found ().

Differences in dry matter production, and essential oil content and yield among oregano populations

The 10 oregano populations (O. vulgare ssp. hirtum), differentiated in their dry matter production, essential oil content and amount of essential oil per pot, in both years of experimentation ( and ). Populations originated from areas 5 and 1 (North-East and South-Pindos floristic areas of Greece, ) produced the highest dry matter in both years of experimentation (63.3 and 60.2 g·pot−1, respectively), showing a superiority of ∼30% compared to the general average of the experiment; while populations 9 and 10 accumulated the lowest dry matter, producing 34.2 and 32.7 g·pot−1, respectively, which was inferior by ∼30% as compared to the general average of the experiment. However, in terms of essential oil content, the highest values were recorded in populations 10 and 9 that originated from the geographical areas Pe and StE, respectively (). The recorded values were ∼2.5-fold higher, compared to the essential oil content of population 1, (namely 5.86, 5.51 and 2.31 ml·100−1 g DW, respectively) for both years. Finally, the total amount of essential oil per pot ranged from 1.37 to 2.46 ml·pot−1, with the highest values recorded in populations 3 and 5, which produced 2.46 and 2.44 ml·pot−1, respectively. On the contrary, the lowest production of essential oil was observed in population 1, which produced only 1.37 ml·pot−1 ( and ).

Table 4. Dry matter (g·pot−1), essential oil content (ml·100−1 g DW) and amount of essential oil per pot (ml·pot−1) of Greek oregano populations in 2012, in 2013 and in over year analysis.

Dry matter production was found to be inversely related to essential oil content. Conclusively populations 5 and 1, belonging to the SPi and NE areas, with the highest dry matter production during plant growth in both years of experimentation () had limited essential oil content, while populations 9 and 10 with the lowest dry matter production had the highest essential oil content. Finally, it was observed that the higher amount of essential oil per pot was produced by populations 3 and 5, which were originated from the NC and SPi areas, respectively ().

Interaction of oregano populations and nitrogen supply levels

Dry matter accumulation and amount of essential oil per pot is of great commercial value and thus, the study of the parameters affecting their production is crucial. Additional nitrogen fertilization of oregano plants up to a certain level was shown to increase their productivity. However, the significant interaction between populations and nitrogen supply levels revealed the different impact of nitrogen to the examined populations. More specifically, regarding the produced dry matter, it was observed that the increased nitrogen supply (level N2) affected positively the accumulated biomass of populations 5, 1, 3, 7, 4 and 6, while an inferior performance was recorded for populations 10, 2, 8 and 9, as compared to the N1 level ((a)).

Figure 2. Interaction of nitrogen supply levels and the Greek oregano populations for (a) dry matter production (g·pot−1), (b) essential oil content (ml·100−1 g DW) and (c) amount of essential oil per pot (ml·pot−1), in 2012 and 2013.

Figure 2. Interaction of nitrogen supply levels and the Greek oregano populations for (a) dry matter production (g·pot−1), (b) essential oil content (ml·100−1 g DW) and (c) amount of essential oil per pot (ml·pot−1), in 2012 and 2013.

Regarding the essential oil content, it was found that the increased nitrogen supply at N2 level had almost no effect on populations 9, 2, 10, 8 and 1 while a clear decline was found for all the other populations by a percentage ranging from 3.4% to 10.7% ((b)).

Finally, the detected interaction concerning the amount of essential oil per pot showed that the further increase of nitrogen supply, from N1 to N2 levels favored populations 1 and 3, which had increased oil yield by 6.8% and 2.4%, respectively. On the contrary, all other populations were not affected positively by the additional nitrogen supply ((c)).

Discussion

It is generally accepted that O. vulgare ssp. hirtum (Greek oregano) has the best quality of the oregano species and important genetic variability for yield and quality was detected in Greece (Lawrence Citation1984; Kokkini and Vokou Citation1989; Vokou et al. Citation1993; Kokkini Citation1997). The essential oil content of O. vulgare ssp. hirtum can reach up to 8%, showing a range from 1.8% to 8.2% (Kokkini & Vokou Citation1989) revealing important genetic potential. In the current work, important variation was identified among the 10 tested populations for dry matter, essential oil content and amount of essential oil per pot in both years of the experimentation, which could be exploited for the development of an oregano breeding program aiming to the production of new cultivars. The populations with the highest dry matter production (1-‘Palaiochori’ and 5-‘Gliki’) and with the highest essential oil content (10-‘Gytheio’ and 9-‘Achladocastro’) were superior by 30%, as compared to the general mean of the experiment, while the populations 3-‘Litochoro’ and 5-‘Gliki’ had the highest amount of essential oil per pot production, increased by 24%, as compared to the general mean of the experiment (). These superior populations could be used in a network of crosses to give desirable progenies, useful as a starting material in a plant breeding program or could be introduced in the cultivation.

Also, it is reported that the climatic characteristics of the environment of origin such as temperature and dryness affects the essential oil content (Vokou et al.Citation1993; Gavalas et al. Citation2011). In our study, the population with the highest essential oil content (10-‘Gytheio’) originated from southern areas (Pe) that are characterized by water scarcity and the highest average annual temperature in combination with the lower precipitation during the cultivation/growing period (March–July), as compared to the other collection sites ( and ). Moreover, the population with the highest dry matter and amount of essential oil per pot (5-‘Gliki’) was originated from an area characterized by high temperature during the cultivation/growing period (March–July), sufficient annual precipitation and limited precipitation during the cultivation/growing period ( and ).

In oregano species, Novak et al. (Citation2003) reported that the genotype is one of the most important factors affecting quality and productivity. These wild oregano genotypes constitute the primary gene pool that could be used at the first stages of a breeding program, since, according to Fehr (Citation1987) this is one of the most important sources of genetic variation.

Our findings showed that, a proposed cross that could give desirable progenies, could take place among populations with high dry matter (5-‘Gliki’) and high essential oil content (10-‘Githeion’ or 9-‘Achladocastro’), as they may combine both desirable productive characters. Moreover, the population 3-‘Litochoro’ is combining high dry matter production and good essential oil content (%), which means that it could be a hopeful starting material to begin within population selection.

Apart the genotypes, other parameters that affect the performance of the cultivated species are the environment and the genotype × environment (G × E) interaction. According to Simmonds (Citation1981), it is estimated that the contribution of the genotype to the yield increase of important economic crops is about 30–60%, of the environment 10–30% and of the interaction G × E 25–45%. So, another target of our experiment was to evaluate the response of the 10 examined populations, under different nitrogen supply levels. Although the impact of nitrogen has been exhaustively investigated in traditional cultivated species, only a few references are reported in the literature regarding oregano (Azizi et al. Citation2009; Sotiropoulou & Karamanos Citation2010). Our findings support that, although oregano is adapted to natural habitats with low nutrient availability, in case of commercial agriculture, where the produced quantity is connected with economic input, a minimum nitrogen supply (N1 level) could be beneficial for the increased dry matter production (). Previous studies have reported similar effects of nitrogen on yield of other Origanum taxa such as Origanum syriacum and Origanum × applii (Omer Citation1999; Barreyro et al. Citation2005; Ozgüven et al. Citation2006) of O. vulgare L. (Azizi et al. Citation2009) and of O. vulgare ssp. hirtum (Link) Ietswaart (Sotiropoulou & Karamanos Citation2010).

Our results showed that although nitrogen supply has positive effect on dry matter production, the opposite impact was found on essential oil content for both years of experimentation (), which could be explained by a higher increase of dry matter production in relation to the corresponding produced amount of oil, as reported by Azizi et al. (Citation2009). Also, the environmental conditions affect essential oil content, as it is recorded from the collection of oregano from natural habitats with different conditions (Kokkini Citation1994; Gavalas et al. Citation2011). Other studies reported a reduction of essential oil content after nitrogen supply in O. vulgare (Azizi et al. Citation2009), in O. syriacum (Omer Citation1999) and in other species of the Lamiaceae family, such as Thymus (Baranauskiene et al. Citation2003) and Rosmarinus (Boyle et al. Citation1991). However, Sotiropoulou and Karamanos (Citation2010) reported no nitrogen effect on oil content in O. vulgare ssp. hirtum (Link) Ietswaart, while positive nitrogen effect on this parameter was reported in Egyptian oregano (O. syriacum) by Ozgüven et al. (Citation2006). Finally, in this work, the total amount of essential oil per pot that is important for commercial production was positively affected by nitrogen supply ( and ). Similar positive effect was reported on the amount of essential oil in many oregano species (Omer Citation1999; Barreyro et al. Citation2005; Ozgüven et al. Citation2006; Azizi et al. Citation2009; Sotiropoulou & Karamanos Citation2010).

The study of the G × E interaction has an important role in the evaluation of the genotypes and has contributed to the development of high-yielding cultivars (Kang Citation2002). However, the interaction of oregano populations and nitrogen supply has not been investigated in depth, since, there are studies that either evaluate only one genotype/population (Omer Citation1999; Barreyro et al. Citation2005; Ozgüven et al. Citation2006; Sotiropoulou & Karamanos Citation2010; Dordas Citation2016) or the G × E interaction was not estimated at all (Azizi et al. Citation2009). So, it should be underlined that in the current work significant interaction between populations and nitrogen supply levels for both years of experimentation was detected, which means that the examined populations responded differently to nitrogen supply ( and ). In addition, when the G × E interaction is repeatable in time as found in our study, it could be exploited in an oregano breeding program (Annicchiarico Citation2009). The results showed that oregano plants required an optimum level of nitrogen supply to maximize the economic results, but this level is differentiated for the populations used in this study. This evidence should be taken into account for further studies to ensure the optimum evaluation of the populations.

Conclusively, the identified variation in Greek oregano genetic resources could be exploited for the development of an oregano breeding program aiming for the production of new cultivars. The proper selection of improved oregano genotypes in combination with optimum level of nitrogen supply might maximize the agricultural potential of sustainable farming systems.

Disclosure statement

No potential conflict of interest was reported by the authors.

Notes on contributors

Elissavet G. Ninou is a postdoc researcher focusing on the evaluation and use of populations for sustainable growth. She has participated in many EU projects and has published research articles on plant breeding and variety water-use efficiency.

Konstantinos A. Paschalidis is a professor of Applications at Technological Educational Institute of Crete, Heraklion, Greece. He has published numerous research articles on arable and horticultural crops, focusing mainly on stress mechanisms and polyamines.

Ioannis G. Mylonas is an expert on plant breeding and biotic and abiotic stress resistance. He has published many works on plant breeding and is currently working on lifelong learning projects of American Farm School. He has participated in many EU projects related to plant breeding and has numerous published research articles.

Christos Vasilikiotis is an assistant professor at the Agro-Environmental Systems Management Department of Perrotis College in Thessaloniki, Greece. He has published articles on molecular biology and photosynthesis research.

Athanasios G. Mavromatis is an assistant professor at the Department of Agricultural Science in Aristotle University of Thessaloniki. Also, he is an invited professor in the MSc Postgraduate program of the Medicine School in the University of Thessaly. He is a specialist in Genetics and Plant Breeding and published in the last 15 years a significant number (>30) of publications on the subjects of plant science, food science and agriculture, organic breeding and exploitation of plant genetic resources.

References

  • Abbad A, Belaqziz R, Bekkouche K, Markouk M. 2011. Influence of temperature and water potential on laboratory germination of two Moroccan endemic thymes: Thymus maroccanus Ball and Thymus broussonetti Boiss. Afr J Agric Res. 6:4740–4745.
  • Adame-Gallegos JR, Andrade-Ochoa S, Nevarez-Moorillon GV. 2016. Potential use of Mexican Oregano essential oil against parasite, fungal and bacterial pathogens. J Essent Oil Bear Pl. 19:553–567. doi: 10.1080/0972060X.2015.1116413
  • Annicchiarico P. 2009. Coping with and exploiting genotype-by-environment interactions. In: Ceccarelli S, Guimarães EP, Weltizien E, editors. Plant breeding and farmer participation. Rome: Food and Agriculture Organization of the United Nations (FAO); p. 519–564.
  • Azizi A, Yan F, Honermeier B. 2009. Herbage yield, essential oil content and composition of three oregano (Origanum vulgare L.) populations as affected by soil moisture regimes and nitrogen supply. Ind Crops Prod. 29:554–561. doi: 10.1016/j.indcrop.2008.11.001
  • Baranauskiene R, Venskutonis PR, Viskelis P, Dambrauskien E. 2003. Influence of nitrogen fertilizers on the yield and composition of Thyme (Thymus vulgaris). J Agric Food Chem. 51:7751–7758. doi: 10.1021/jf0303316
  • Baratta TM, Dorman DHJ, Deans SG, Biondi DM, Ruberto G. 1998. Chemical composition, antimicrobial and antioxidative activity of laurel, sage, rosemary, oregano and coriander essential oils. J Ess Oil Res. 10:618–627. doi: 10.1080/10412905.1998.9700989
  • Barreyro R, Ringuelet J, Agricola S. 2005. Nitrogen fertilization and yield in oregano (Origanum×applii). Ciencia Invest Agrar. 32:34–38.
  • Bilalis D, Katsenios N, Efthimiadou A, Efthimiadis P., Karkanis A. 2012. Pulsed electromagnetic fields effect in oregano rooting and vegetative propagation: a potential new organic method. Acta Agr Scand B.-S. P. 62:94–99.
  • Boyle TH, Cracker LE, Simon JE. 1991. Growing medium and fertilization regime influence growth and essential oil content of rosemary. Hort Sci. 26:33–34.
  • Chatzopoulou PS, Koutsos TV, Katsiotis ST. 2004. Determination of the essential oil content and composition of some Origanum species cultivated in Greece. In: Proceedings of 3rd conference on medicinal and aromatic plants of southeast European countries; 2004 September 5–8; Nitra, Slovak Republic, 55–56.
  • Costa AG, Bertolucci SKV, Changas JH, Ferraz EO, Pinto JEP. 2013. Biomass production, yield and chemical composition of peppermint essential oil using different organic fertilizer sources. Cienc Agrotec. 37:202–210. doi: 10.1590/S1413-70542013000300002
  • De Falco E, Roscigno G, Landolfi S, Scendolera E, Senatore F. 2014. Growth, essential oil characterization, and antimicrobial activity of three wild biotypes of oregano under cultivation condition in Southern Italy. Ind Crop Prod. 62:242–249. doi: 10.1016/j.indcrop.2014.08.037
  • Dordas CA. 2009. Foliar application of calcium and magnesium improves growth, yield, and essential oil yield of oregano (Origanum vulgare ssp. hirtum). Ind Crops Prod. 29:599–608. doi: 10.1016/j.indcrop.2008.11.004
  • Dordas CA. 2016. Chlorophyll meter readings, N leaf concentration and their relationship with N use efficiency in oregano. J Plant Nutr. doi:10.1080/01904167.2016.1240200
  • EDQM. 2005. European pharmacopoeia. 5th ed. Strasbourg: Council of Europe.
  • Fehr WR. 1987. Principles of cultivar development, Vol. 1: Theory and Technique. Eds by Macmillan Publishing Company, A Division of Macmillan, Inc. 866 Third Avenue, New York, NY. 10022.
  • Gavalas NP, Kalburtji KL, Kokkini S, Mamolos AP, Veresoglou DS. 2011. Ecotypic variation in plant characteristics for Origanum vulgare subsp. hirtum populations. Biochem Syst Ecol. 39:562–569. doi: 10.1016/j.bse.2011.08.007
  • Gavaric N, Mozina S, Kladar N, Bozin B. 2015. Chemical profile, antioxidant and antibacterial activity of Thyme and Oregano essential oils, Thymol and carvacrol and their possible synergism. J Essent Oil Bear Pl. 18:1013–1021. doi: 10.1080/0972060X.2014.971069
  • Jamali CA, Kastrati A, Bekkouche K, Hassani L, Wohlmuth H, Leach D, Abbad A. 2014. Cultivation and the application of inorganic fertilizer modifies essential oil composition in two Moroccan species of Thymus. Ind Crops Prod. 62:113–118. doi: 10.1016/j.indcrop.2014.08.017
  • Johnson CB, Kazantzis A, Skoula M, Mitteregger U, Novak J. 2004. Seasonal population and ontogenic variation in the volatile oil content and composition of individuals of Origanum vulgare subsp. hirtum, assessed by GC head space analysis and by SPME sampling of individual oil glands. Phytochem Anal. 15:286–292. doi: 10.1002/pca.780
  • Kang MS. 2002. Genotype-environment interaction: progress and prospects. In: Kang MS, editor. Quantitative genetics, genomics and plant breeding. Wallingford (UK): CABI; p. 221–243.
  • Karamanos AJ, Sotiropoulou DE. 2013. Field studies of nitrogen application on Greek oregano (Origanum vulgare ssp. hirtum (Link) Ietswaart) essential oil during two cultivation seasons. Ind Crops Prod. 46:246–252. doi: 10.1016/j.indcrop.2013.01.021
  • Kintzios SE. 2002. Profile of the multifaceted prince of the herbs. In: Kintzios SE, editor. Oregano: the genera Origanum and Lippia. London: Taylor and Francis; p. 3–8.
  • Kizil S, Ipekb A, Arslanc N, Mahmood Khawar K. 2009. Some agronomical characteristics and essential oil content of oregano (Origanum onites L.) as influenced by planting densities. J Essent Oil Bear Pl. 12:172–180. doi: 10.1080/0972060X.2009.10643707
  • Kokkini S. 1994. Herbs of the Labiatae. In: Macrae R, Robinson R, Sadlerand M, Fullerlove G, editors. Encyclopedia of food science, food technology and nutrition. London: Academic Press; p. 2342–2348.
  • Kokkini S. 1997. Taxonomy, diversity and distribution of Origanum species. In: Padulosi S, editor. Proceedings of the IPGRI International Workshop on Oregano; 1996 May 8–12; CIHEAM, Valenzano (Bari), Italy, IPGRI.
  • Kokkini S, Karousou R, Vokou D. 1994. Pattern of geographic variation of Origanum vulgare trichomes and essential oil content in Greece. Biochem Syst Ecol. 22:517–528. doi: 10.1016/0305-1978(94)90046-9
  • Kokkini S, Vokou D. 1989. Carvacrol-rich plants in Greece. Flav Frag. J. 4:1–7. doi: 10.1002/ffj.2730040102
  • Lawrence BM. 1984. The botanical and chemical aspects of oregano. Perfum Flav. 9:41–51.
  • Novak J, Grausgruber H, Pank F, Langbehn J, Blόthner WD, Vender C, Niekerk LV, Junghanns W, Franzl C. 2003. Stability of hybrid combinations of marjoram (Origanum majorana L.). Flav Frag J. 18:401–406. doi: 10.1002/ffj.1233
  • Omer AE. 1999. Response of wild Egyptian oregano to nitrogen fertilization in a sandy soil. J Plant Nutr. 19:955–967.
  • Ozgüven M, Ayanoglu F, Ozel A. 2006. Effects of nitrogen rates and cutting times on the essential oil yield and components of Origanum syriacum L. var. bevanii. J Agron. 5:101–105. doi: 10.3923/ja.2006.101.105
  • Rhayour K, Bouchikhi T, Tantaoui-Elaraki A, Sendide K, Remmal A. 2003. The mechanism of bactericidal action of oregano and clove essential oils and of their phenolic major components on Escherichia coli and Bacillus subtilis. J Ess Oil Res. 15:356–362. doi: 10.1080/10412905.2003.9698611
  • Said-Al Ahl HAH, Omer EA, Naguib NY. 2009. Effect of water stress and nitrogen fertilizer on herb and essential oil of oregano. Int Agrophys. 23:269–275.
  • Simmonds NW. 1981. Genotype (G), environment (E) and GE components of crop yields. Exp Agric 17:355–362. doi: 10.1017/S0014479700011807
  • Skoula M, Harborne JB. 2002. The taxonomy and chemistry of Origanum. In: Kintzios SE, editor. Oregano: the genera Origanum and Lippia. London: Taylor and Francis; p. 67–108.
  • Sotiropoulou DE, Karamanos A. 2010. Field studies of nitrogen application on growth and yield of Greek oregano (Origanum vulgare ssp. hirtum (Link) Ietswaart). Ind Crops Prod. 32:450–457. doi: 10.1016/j.indcrop.2010.06.014
  • Strid A, Tan K. 2002. Flora Hellenica Vol. 2. A.R.G. Gantner Verlag K.G., p. X–XI.
  • Vokou D, Kokkini S, Bessiere JM. 1993. Geographic variation of Greek oregano (Origanum vulgare spp. hirtum) essential oils. Biochem Syst Ecol. 21:287–295. doi: 10.1016/0305-1978(93)90047-U

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.