Changes in the essential oil yield and composition of dill (Anethum graveolens L.) as response to arbuscular mycorrhiza colonization and cropping system

Industrial Crops and Products 77 (2015) 295–306

Contents lists available at ScienceDirect

Industrial Crops and Products journal homepage: www.elsevier.com/locate/indcrop

Changes in the essential oil yield and composition of dill (Anethum graveolens L.) as response to arbuscular mycorrhiza colonization and cropping system Weria Weisany a,∗ , Yaghoub Raei a , Ilaria Pertot b a b

Department of Plant Ecophysiology, Faculty of Agriculture, Tabriz University, Iran Safe Crop Centre, Istituto Agrario di S. Michele all’Adige, Via Mach 1, S. Michele all’Adige, Trento 38010, Italy

a r t i c l e

i n f o

Article history: Received 7 June 2015 Received in revised form 23 August 2015 Accepted 1 September 2015 Keywords: Cropping system Essential oil Funneliformis mosseae Land equivalent ratio Medicinal plant

a b s t r a c t Intercropping and arbuscular mycorrhizal (AM) fungi application are thought to be useful means of minimizing the risks of agricultural production in many environments. Hence, this work was conducted to study and compare the effectiveness of AM fungi (Funneliformis mosseae) on growth, chlorophyll content, shoot water content, land equivalent ratio (LER) and essential oil (EO) yield and composition of dill in different cropping systems. Two experiments were carried out with factorial arrangement based on randomized complete block design with three replications in 2013 and 2014. The factors were cropping systems including (a) common bean (Phaseolus vulgaris L.) sole cropping (40 plants m−2 ), (b) dill (Anethum graveolens L.) sole cropping at different densities (25, 50 and 75 plants m−2 ) and (c) the additive intercropping of dill + common bean (25+40, 50+40 and 75+40 plants m−2 ). All these treatments were applied with (+AM) or without (−AM) arbuscular mycorrhiza colonization. In both cropping systems, the AM colonization significantly increased chlorophyll content, LER and EO yield as compared to non-inoculated plants. Changes in EO composition were detected in inoculated and intercropped dill plants. The content of ␣-phellandrene, limonene, ␤-phellandrene, terpinen-4-ol, cryptone and carvone were enhanced in EO obtained from AM-inoculated and intercropped dill plants, while AM colonization resulted in a lesser content of ␣-terpinene, p-cymene, ␣-terpinolene, p-␣-dimethylstyrene, dill ether, n-dihydrocarvone and cis-sabinol at sole cropped dill plants. © 2015 Elsevier B.V. All rights reserved.

1. Introduction Intercropping is an old and widespread practice used in low input cropping systems in many areas of the world (Anil et al., 1998). Currently, this system is attracting increasing interesting in low-input crop production systems and is being extensively investigated (Zhang and Li, 2003; Zuo et al., 2003; Li et al., 2004). The advantages of intercropping have been demonstrated in numerous systems (Ghosh, 2004). Small-scale farmers practice intercropping to obtain greater total land productivity, expressed by the land equivalent ratio (LER) (Songa et al., 2007). The benefits of intercropping include improvement of soil fertility (because of greater biomass production, nutrient cycling and biological nitrogen fixation), soil physical conditions (because of organic matter

∗ Corresponding author at: Young Researchers and Elite Club, Islamic Azad University, Sanandaj Branch, Sanandaj, Iran. E-mail address: [email protected] (W. Weisany). http://dx.doi.org/10.1016/j.indcrop.2015.09.003 0926-6690/© 2015 Elsevier B.V. All rights reserved.

aggregation, humic acid and glomalin production, and root activity), and soil erosion control. In general, intercropping has been shown to be more productive than sole cropping. Medicinal plants play major roles in human health services worldwide. Many people in both developing and developed countries are turning to herbal medicine (Wondimu et al., 2007). Furthermore, some essential oil (EO) composition of the medicinal plants used in industrial. For example, carvone was identified as an effective potato sprout inhibitor (Hartmans et al., 1995), in addition it can also inhibit the growth of certain fungi (Farag et al., 1989) and microorganisms (Vokou et al., 1993) and it can act as an insect repellent (Su, 1985). Besides carvone, myristicin and apiole were also identified as natural insecticides (Duke, 2001). Little research has been carried out on intercropping medicinal and leguminous plants. Previous results regarded the qualitative aspect of production with intercropping, and it has been demonstrated that in some cases this technique may affect the chemical features of the consociated species, causing variations both in the total yield of EO and in the chemical composition of the extracts.

296

W. Weisany et al. / Industrial Crops and Products 77 (2015) 295–306

For example, the alkaloid content in jimson weed (Datura stramonium L.) seems to be affected by the cultivation of other species nearby, showing, respectively, an enhancement with lupine (Lupinus albus L.) or a decrease with peppermint (Mentha piperita L.) (Morelli, 1981). The EO content of peppermint is furthermore positively affected by intercropping with soybean (Glycine max Merr.), which also increases the menthol content of peppermint oil (Maffei and Mucciarelli, 2003). The roots of many plant species live in symbiosis with certain soil fungi (Mycorrhizae). Although underestimated in the past, mycorrhizal symbioses now known to be important for a sustainable management of agricultural ecosystems (Jeffries et al., 2003; Barrios, 2007; Smith and Read, 2008). Many aspects of the interaction between plants and arbuscular mycorrhizal (AM) fungi were studied (growth effect, nutritional exchanges, tolerance to stressful conditions), but little is known about the potential of AM fungi to affect the accumulation and composition of secondary metabolites of medicinal plants. Several reports have investigated secondary compound patterns of mycorrhized roots such as phenolic compounds (Devi and Reddy, 2002; Rojas-Andrade et al., 2003), alkaloids (Rajeshkumar et al., 2008) and isoprenoids (Kapoor et al., 2007; Rapparini et al., 2008). Reported results include the increased production of EO in coriander and Anethum graveolens L. colonized by Glomus fasciculatum or Glomus macrocarpum (Kapoor et al., 2002a,b), in mint colonized by G. fasciculatum or a suite of AM fungi (Gupta et al., 2002; Freitas et al., 2004), in sweet basil colonized by Gigaspora rosea (Copetta et al., 2006), in oregano colonized by Funneliformis mosseae (Khaosaad et al., 2006) and in annual wormwood colonized by G. fasciculatum (Kappoor et al., 2007; Chaudhary et al., 2008). Rasouli-Sadaghianil et al. (2010) showed that G. fasciculatum may have a higher symbiotic potential in increasing EO contents in basil. Kapoor et al. (2004) also reported that G. fasciculatum and G. macrocarpum on Foeniculum vulgare, significantly enhanced the accumulation of EO. Arbuscular mycorrhizae improve plant development, nutrition and EO content (Nell et al., 2010). Symbiosis between plants and AM fungi can promote the accumulation of several secondary metabolites in medicinal plants which play important roles in treating human diseases (Kapoor et al., 2002a,b). Recently, Adams et al. (2004) observed that EO levels in vetiver roots are modulated in the presence of nonidentified bacteria and fungi, and AM were suggested to be involved in the altered EO accumulation. Freitas et al. (2004) also indicated that inoculation with AM fungi led to an increase of 89% in the EO and menthol contents of Mentha arvensis plants. In studies on Ocimum basilicum (Copetta et al., 2006) and M. arvensis (Freitas et al., 2004), it was shown that AM fungal root colonization increases the EO content and in O. basilicum alterations of the EO composition have been reported (Copetta et al., 2006). Also, Mucciarelli et al. (2003) observed that colonization by an endophytic, non-mycorrhizal fungus increased development and altered the composition of the essential oils in M. piperita. AM fungi can influence the production of active ingredients in medicinal and aromatic plants (Kapoor et al., 2002; Karagiannidis et al., 2011), resulting from a better nutritional conditional or by means of protecting the host to the presence of the fungus (Volpin et al., 1994). In Artemisia annua, Rapparini et al. (2008) reported that mycorrhization did not influence the amount of total terpenes, while it did affect single terpene production and emission.

The accumulation of flavonoids (Larose et al., 2002), cyclohexanone derivatives and apocarotenoids (Fester et al., 2002; Vierheilig et al., 2000a,b), phytoalexins (Yao et al., 2003), phenolic compounds (Devi and Reddy, 2002), triterpenoids (Akiyama and Hayashi, 2002), and glucosinolates (Vierheilig et al., 2000c) in plants colonized by AM fungi has been reported. Khaosaad et al. (2006) observed that EO levels in Origanum species are increased in the presence of AM fungi. The hypotheses of this experiment are: (1) AM fungi increase chlorophyll content and growth of intercropped plants and this, in turn, will increase the crop production. (2) Intercropping and AM colonization produce greater changes than sole cropping and non-AM colonization in EO quantity and quality of dill. While intercropping and AM symbiosis can increase the contents of some secondary metabolites of medicinal plants, it is not clear whether the composition of the secondary metabolites in medicinal plants also changes. To the best of our knowledge there are no reports on effect of intercropping and AM fungi on the quantity and quality of EO in dill plants. Thus, our aims were: (1) to understand the combined effects of both intercropping and AM fungi (F. mosseae) colonization on plant growth, chlorophyll and shoot water content of common bean and dill, (2) to investigate the effects of AM colonization on qualitative and quantitative synthesis of the EO of dill (A. graveolens L.) intercropped with common bean, (3) to evaluate the benefit effects of intercropping and F. mosseae colonization, in relation to sole cropping through the LER. 2. Materials and methods 2.1. Experimental design Two field experiments were conducted in the Agriculture and Natural Resources Research Center of Kurdistan Province in 2013 and 2014. For the soil analysis soil samples (from 10 to 15 cm depth) were randomly collected in 2013 from eight points using a soil auger. Other soil samples were taken from plots with different treatments at harvest time. All soil samples were air dried at laboratory for 3 days and then crushed and sieved through a 2 mm sieve. Subsequently, various chemical and physical properties of soils were determined (Table 1). The experiments were carried out with a factorial arrangement based on randomized complete block design with three replications. The factors were cropping systems including: (a) common bean (Phaseolus vulgaris L.) sole cropping (C40 = 40 plants m−2 ), (b) dill (Anethum graveolens L.) sole cropping at different densities (D25, D50 and D75: 25, 50 and 75 plants m−2 , respectively) and (c) the additive intercropping of dill + common bean (25 + 40, 50 + 40 and 75 + 40 plants m−2 ). All these treatments were applied with (+AM) or without (−AM) arbuscular mycorrhiza colonization. The size of each plot was 4 m × 5 m. The experimental site has been previously cultivated with a pea–wheat–oilseed rape rotation. Oilseed rape (Brassica napus L.) was grown in 2012. Primary tillage was conducted in the third week of October 2012 and 2013. A mounted moldboard plow (3 bottoms with a 30 cm working width) was used for primary tillage in April. Secondary tillage was performed by a tandem disk harrow (20 disks with a 530 mm diameter, 5 each in 4 rows and working width of 1400 mm) in the same direction of plowing. The soil contained efficient populations of native Rhizobium gallicum because plants have been nodulated. The crops were

Table 1 Some physical and chemical properties of the soil of experimental area. Texture

Organic carbon %

pH (1:2.5)

Electrical conductivity (dS m−1 ) (1:2.5)

K P (mg kg−1 soil)

Ca

Na

Zn

Mn

Fe

Cu

Sandy clay loam

1.14

7.12

0.072

131

1150.1

450.2

0.476

7.054

6.97

0.826

12.2

W. Weisany et al. / Industrial Crops and Products 77 (2015) 295–306

managed according to organic farming practices without pesticide or fertilizer use. No mechanical weeding was performed after sowing. The AM inoculum consisted of colonized root fragments, sand, AM hyphae, and spores. The inoculum was mixed with an inert material for dilution and homogenizing the distribution in the soil. A 30-g portion of inoculum was added to each plot at sowing time just below the seeds. The AM fungus (F. mosseae strain of BEG 119) was obtained from the culture collection of University of Tabriz, Iran. 2.2. Plant growth measurements and chlorophyll content

297

LER needed to grow either crops or cultures together compared to the amount of land needed to grow a pure stand of each. To calculate the LER, the intercrop yield of one culture is divided by the yield of the pure stand (Mead and Willey, 1980). In this study we used seed weight as yield parameter. LER = (Yab/Ya) + (Yba/Yb), where Ya and Yb are the yields of common bean and dill, respectively, as sole crops and Yab and Yba are the yields of common bean and dill, respectively, as intercrops. LER values >1 indicate an advantage from intercropping, in terms of the use of environmental resources for plant growth, and when LER < 1 resources are used more efficiently by sole cropping than by intercropping (Vandermeer, 1989).

The plants (four-months-old) were collected from 1 m2 of each plot. In the sampling plots, the randomly chosen plants from each treatment were harvested along with complete roots, and the plant biomass (fresh weight) was recorded. The chlorophyll status of the dill and common bean plants was evaluated in each plot by SPAD analysis (SPAD 502, Minolta Ltd., Osaka, Japan). In both years, SPAD measurements were performed at the time of flowering stage. For each sampled leaf, the average of three random SPAD measurements carried out on the middle part of the leaf blade was recorded.

2.5. Essential oil isolation

2.3. Shoot water content

2.6. Gas chromatography–mass spectrometry

At the flowering stage, water content (WC) was assessed in shoots of all experimental groups. Biomass was estimated for shoot fresh (FM) and dry matter (DM). Plant samples were dried at 70 ◦ C for 48 h until reaching a constant mass in order to measure quantitatively the DM. The WC in the shoots was calculated as: WC = (FM − DM)/DM.

Gas chromatography (GC) analysis was performed using a Trace GC Ultra gas chromatograph coupled with a TSQ Quantum Tandem mass spectrometer, upgraded to the XLS configuration. A DuraBrite IRIS ion source with pre-filter was installed to improve the performance of the spectrometer. The system was equipped with a Triplus auto sampler (Thermo Electron Corporation, Waltham, MA). The injection volume was 1 ␮L, post injection dwell time 4 s, tray temperature 7 ◦ C. GC separation was performed on a 30 m VF-WAXms cappillary column with an internal diameter of 0.25 mm and a film thickness of 0.25 ␮m (Varian, Inc., USA). Temperature programmer: 40 ◦ C hold for 4 min after injection, 6 ◦ C/min up to 250 ◦ C hold for 5 min. Injection parameters were: split injection, split ratio 100:1,

2.4. Land equivalent ratio LER was used to compare intercropped and sole cropped growth. A LER is an indicator for comparing and estimating the benefit of various ways of managing intercropped plots. It is defined as the

At the beginning of flowering, leaves and shoots of dill were harvested, and the EOs were obtained by hydrodistillation in 500 mL H2 O in a Clevenger apparatus for 2 h. The obtained distillate was extracted using diethyl–ether as solvent (1/1, v/v) and dried over anhydrous sodium sulphate. The organic layer was then concentrated at 35 ◦ C using a Vigreux column and the EO stored at 4 ◦ C prior to analysis. The shoot essential oil yield measured in liter per hectare (L/h).

Table 2 Fresh weight of common bean and dill inoculated (+AM) and non-inoculated with arbuscular mycorrhiza (−AM) in sole and intercropping systems in 2013 and 2014. Fresh weight (g m−2 )

Treatments

2013

2014

Common bean

Dill

Common bean

Dill

Intercropping

D75/C40 D75/C40 D50/C40 D50/C40 D25/C40 D25/C40

−AM +AM −AM +AM −AM +AM

365.3 ± 11 400.6 ± 51 396.6 ± 190 422.0 ± 202 388.0 ± 98 484.0 ± 143

484.6 ± 55 572.6 ± 96 382.0 ± 139 462.6 ± 195 348.0 ± 83 484.0 ± 102

749.3 ± 161 955.3 ± 151 600.6 ± 231 757.3 ± 96 660.0 ± 48 790.6 ± 134

803.0 ± 317 823.1 ± 228 703.2 ± 205 1073.3 ± 245 716.2 ± 225 785.1 ± 412

Sole cropping

C40 C40 D75 D75 D50 D50 D25 D25

−AM +AM −AM +AM −AM +AM −AM +AM

352.0 ± 51 414.0 ± 48 – – – – – –

– – 327.3 ± 7 453.3 ± 96 450.6 ± 189 504.0 ± 72 480.6 ± 88 570.6 ± 111

648.0 ± 199 848.0 ± 197 – – – – – –

– – 781.4 ± 190 1215.3 ± 336 953.2 ± 220 62.2 ± 125 427.4 ± 23 598.2 ± 62

** NS NS ** NS

** *** *** *** NS

** NS NS ** NS

** *** *** *** NS

Year Repetition (year) CS AM CS*AM

+ Comparison of means among cropping systems (CS), arbuscular mycorrhiza (AM) and interaction of cropping systems × arbuscular mycorrhiza (CS*AM) (P ≤ 0.05). Results are the mean of three replications ± SD. NS, *, **, ***: non-significant and significant at P ≤ 0.05, P ≤ 0.01 and P ≤ 0.001, respectively. C40: sole cropping of common bean (40 plants m−2 ). D25, D50 and D75: sole cropping of dill at 25, 50 and 75 plants m−2 , respectively. D/C: dill/common bean intercropping. +AM, −AM: with and without arbuscular mycorrhiza colonization, respectively.

298

W. Weisany et al. / Industrial Crops and Products 77 (2015) 295–306

Table 3 Shoot water and chlorophyll contents of common bean and dill shoots inoculated (+AM) and non-inoculated with arbuscular mycorrhiza (−AM) in sole and intercropping systems in 2013 and 2014. Treatments

Shoot water content (%) 2013

Chlorophyll content (SPAD) 2014

2013

2014

Common bean

Dill

Common bean

Dill

Common bean

Dill

Common bean

Dill

Intercropping

D75/C40 D75/C40 D50/C40 D50/C40 D25/C40 D25/C40

−AM +AM −AM +AM −AM +AM

78.92 ± 0.66 72.56 ± 13.51 65.93 ± 12.02 78.03 ± 5.13 74.52 ± 2.57 64.46 ± 17.47

71.33 ± 3.51 67.05 ± 8.26 70.09 ± 2.07 65.17 ± 10.45 70.02 ± 2.79 71.21 ± 3.14

77.55 ± 1.93 78.87 ± 1.38 77.78 ± 0.98 73.39 ± 10.56 75.25 ± 1.67 78.32 ± 1.27

77.49 ± 1.48 76.46 ± 5.15 74.07 ± 1.58 79.01 ± 1.77 76.69 ± 0.73 76.26 ± 4.65

50.20 ± 2.35 42.97 ± 3.12 46.47 ± 4.05 44.50 ± 5.74 53.97 ± 3.58 45.07 ± 2.20

10.0 ± 4.28 6.40 ± 1.74 7.40 ± 2.61 4.70 ± 1.74 8.23 ± 1.59 6.47 ± 2.83

49.77 ± 1.82 42.37 ± 6.04 50.03 ± 1.40 46.13 ± 4.77 49.63 ± 3.48 50.80 ± 2.86

10.03 ± 2.84 5.90 ± 2.35 9.27 ± 5.84 4.83 ± 2.58 8.20 ± 3.90 3.83 ± 0.31

Sole cropping

C40 C40 D75 D75 D50 D50 D25 D25

−AM +AM −AM +AM −AM +AM −AM +AM

74.70 ± 4.63 79.91 ± 4.82 – – – – – –

– – 69.01 ± 4.90 71.35 ± 3.09 72.51 ± 0.49 73.06 ± 7.38 69.18 ± 9.68 71.49 ± 0.65

79.58 ± 2.19 76.18 ± 6.28 – – – – – –

– – 76.33 ± 2.59 78.56 ± 4.89 78.15 ± 6.17 77.52 ± 2.23 77.57 ± 2.07 76.68 ± 1.77

47.57 ± 1.67 39.80 ± 4.52 – – – – – –

– – 6.67 ± 2.47 5.33 ± 2.06 11.1 ± 5.86 5.23 ± 1.14 10.5 ± 0.89 5.33 ± 2.38

49.40 ± 3.10 38.55 ± 3.95 – – – – – –

– – 7.47 ± 3.42 5.07 ± 3.42 7.73 ± 2.90 5.23 ± 1.51 8.00 ± 2.59 5.57 ± 1.29

NS * NS NS NS

NS NS NS NS NS

NS NS NS NS NS

NS NS NS NS NS

NS NS ** *** NS

NS *** NS *** NS

NS NS NS ** NS

NS * NS *** NS

Year Repetition (year) CS AM CS*AM

+ Comparison of means among cropping systems (CS), arbuscular mycorrhiza (AM) and interaction of cropping systems × arbuscular mycorrhiza (CS*AM) (P ≤ 0.05). Results are the mean of three replications ± SD. NS, *, **, ***: non-significant and significant at P ≤ 0.05, P ≤ 0.01 and P ≤ 0.001, respectively. C40: sole cropping of common bean (40 plants m−2 ). D25, D50 and D75: sole cropping of dill at 25, 50 and 75 plants m−2 , respectively. D/C: dill/common bean intercropping. +AM, −AM: with and without arbuscular mycorrhiza colonization, respectively.

inlet temperature 250 ◦ C, carrier gas was helium 5.5, constant flow: 1.2 mL/min. The mass spectrometry was used in scan mode in the range 40–400 m/z with a scan time of 0.200 s. The ionization mode was electron impact (EI) and the source temperature was kept at 250 ◦ C. The chemical components of dill extracts were determined by comparison of their GC retention indices and mass spectra with those reported in the Wiley 5 library and the Adam library (2008). 2.7. Arbuscular mycorrhizal fungi colonization The root samples were extracted by using a cylindrical corer (10 mm). The soil was removed by soaking the roots in water and gently washing them, to ensure that all the thinner roots and tips remained intact. The staining procedure was applied according to Vierheilig et al. (2005) with the modified parameters for the present study. The roots were cut into small pieces (1 cm) and placed in a beaker (10% KOH) for 60 min in a water bath at 65 ◦ C. The roots were then rinsed with tap water and acidified with 5% lactic acid at room temperature for 12 h. Finally, the roots were stained by a solution containing 875 mL lactic acid, 63 mL glycerin, 63 mL tap water and 0.1 g acid fuchsine for 30 min at 70 ◦ C and then de-stained in laboratory by lactic acid for 15 min. Ten root segments were mounted onto slides and examined at 100-400 magnification under a Nikon YS100 microscope. Beneath the glass slide an acetate film with 10 thin lines was adapted. At crossing points between roots and lines, each point that had an infection was recorded and the number of infections was expressed as percentage. The percentage of mycorrhizal root colonization was calculated (McGonigle et al., 1990). 2.8. Statistical analysis Three-way ANOVA was used to determine whether differences in cropping systems or micorrhizal colonization existed between treatments in two years. Combined analysis of variance was performed using SAS version 9.1 (SAS Institute Inc., Cary, NC, USA) (SAS Institute Inc., 1988). Means of the treatments were compared, using Generalized Linear Model (GLM) method and the least significant

difference (LSD) test at the 5% probability level. The data showed normal distribution and no transformation was required. 3. Results 3.1. Arbuscular mycorrhizal colonization Natural AM colonization was observed in all plant species and root samples; however, the percentage of mycorrhizal root colonization was significantly (P ≤ 0.01) greater in all the plants that have been inoculated with AM than in the non-inoculated controls. There were no significant differences in colonization rates of sole and intercropping systems (Fig. 1). 3.2. Fresh weight Fresh weight was significantly influenced by cropping systems (P ≤ 0.01) (Table 2). Dill + common bean intercropping increased fresh weight compared with sole crops in 2013 and 2014 (Table 2). Dill fresh weight was affected by AM colonization and different cropping systems, so that in intercropping, the inoculated plants with F. mosseae had more, but non-inoculated plants had less fresh weight. In both years, differences between fresh and dry weights were similar, so the data for dry weight were not presented. 3.3. Shoot water content There was no significant difference between sole and intercropped plants in shoot water content (Table 3). Also, there was no noticeable difference between non-inoculated plants and those inoculated with F. mosseae. 3.4. Chlorophyll content In 2013, leaf chlorophyll content of common bean were higher under intercropping than under sole cropping systems, so that chlorophyll content increased in dill + common bean intercropping

W. Weisany et al. / Industrial Crops and Products 77 (2015) 295–306

299

Fig. 1. Root colonization percentage in common bean and dill sole and intercrops inoculated and non-inoculated with arbuscular mycorrhiza (Funneliformis mosseae). Results are the mean of three replications ± SD. P < 0.05. C40: sole cropping of common bean (40 plants m−2 ). D25, D50 and D75: sole cropping of dill at 25, 50 and 75 plants m−2 , respectively. D + C: dill + common bean intercropping.

Fig. 2. Partial land equivalent ratio (LER) of common bean (A) and dill (B) inoculated (M) and non-inoculated (non-m) with arbuscular mycorrhiza (Funneliformis mosseae) in 2013 and 2014. Results are the mean of three replications ± SD. P < 0.05. D/C: The additive intercropping of dill + common bean (25 + 40, 50 + 40 and 75 + 40 plants m−2 ).

300

Table 4 Chemical composition (% of essential oil) of essential oils of dill shoots inoculated (+AM) and non-inoculated with arbuscular mycorrhiza (−AM) in sole and intercropping systems. Sole cropping

Intercropping D75/C40 −AM

D75/C40 +AM

D50/C40 −AM

D50/C40 +AM

D25/C40 −AM

D25/C40 +AM

D75 −AM

D75 +AM

D50 −AM

D50 +AM

D25 −AM

D25 +AM

Confirmed by

␣-Pinene ␣-Phellandrene ␣-Terpinene Limonene ␤-Phellandrene P-cymene ␣–Terpinolene P-␣–dimethylstyrene (p-cymenene) Dill ether (3,9-epoxy-1-p-menthene; anethofuran) Trans-3(10)-caren-2-ol Trans-p-2-menthen-1-ol 1-Terpineol (terpinene-1-ol) Terpinen-4-ol (4-terpineol) N-dihydrocarvone (trans-dihydrocarvone) Iso-dihydrocarvone (cis-dihydrocarvone) Cryptone Carvone Cis-Piperitol (cis-p-menth-1-en-3-ol) Cis-sabinol P-cymen-8-ol Carvacrol Myristicin Dill apiole (dillapiole; dillapiol) Apiole

0.03 ± 0.00 2.26 ± 0.08 0.17 ± 0.01 1.63 ± 0.09 1.51 ± 0.11 4.64 ± 0.22 0.05 ± 0.00 0.04 ± 0.00

0.33 ± 0.01 12.68 ± 0.19 0.89 ± 0.05 6.83 ± 0.25 3.12 ± 0.08 6.80 ± 0.14 0.07 ± 0.00 0.06 ± 0.01

0.04 ± 0.00 1.93 ± 0.04 0.51 ± 0.02 1.97 ± 0.04 1.31 ± 0.02 5.76 ± 0.09 0.05 ± 0.00 0.06 ± 0.00

0.05 ± 0.00 2.12 ± 0.14 0.46 ± 0.03 2.06 ± 0.14 1.38 ± 0.10 5.90 ± 0.37 0.05 ± 0.00 0.05 ± 0.00

0.05 ± 0.00 1.92 ± 0.07 0.56 ± 0.02 2.01 ± 0.06 1.29 ± 0.03 5.88 ± 0.15 0.05 ± 0.00 0.07 ± 0.00

0.01 ± 0.00 1.28 ± 0.04 0.05 ± 0.00 0.99 ± 0.03 0.87 ± 0.02 2.82 ± 0.08 0.03 ± 0.00 0.01 ± 0.00

0.03 ± 0.00 1.80 ± 0.06 1.47 ± 0.05 1.97 ± 0.06 0.94 ± 0.04 7.10 ± 0.20 0.06 ± 0.00 0.32 ± 0.01

0.05 ± 0.01 2.25 ± 0.07 0.55 ± 0.02 2.36 ± 0.06 1.55 ± 0.04 6.94 ± 0.17 0.06 ± 0.00 0.07 ± 0.00

0.00 ± 0.00 0.85 ± 0.04 2.19 ± 0.06 1.93 ± 0.05 0.11 ± 0.02 11.44 ± 0.33 0.55 ± 0.01 0.72 ± 0.01

0.02 ± 0.00 1.50 ± 0.07 0.05 ± 0.00 1.06 ± 0.05 0.93 ± 0.05 2.85 ± 0.13 0.02 ± 0.00 0.01 ± 0.00

0.02 ± 0.00 1.36 ± 0.02 2.80 ± 0.17 2.19 ± 0.11 0.58 ± 0.02 8.28 ± 0.45 0.12 ± 0.01 0.54 ± 0.02

0.00 ± 0.00 0.76 ± 0.07 2.31 ± 0.15 1.53 ± 0.10 0.27 ± 0.00 6.10 ± 0.36 0.11 ± 0.00 0.26 ± 0.01

STD, MS STD, MS RI, MS STD, MS RI, MS STD, MS STD, MS STD, MS

23.58 ± 0.66

21.53 ± 0.27

19.68 ± 0.22

18.35 ± 0.49

18.03 ± 0.19

18.50 ± 0.41

16.49 ± 0.34

18.58 ± 0.24

22.35 ± 0.32

18.92 ± 0.39

24.26 ± 0.52

19.69 ± 0.49

RI, MS

0.00 ± 0.00 0.00 ± 0.00 0.00 ± 0.00 0.19 ± 0.00 2.05 ± 0.07

0.00 ± 0.00 0.00 ± 0.00 0.00 ± 0.00 0.23 ± 0.01 1.07 ± 0.06

0.00 ± 0.00 0.14 ± 0.01 0.00 ± 0.00 0.09 ± 0.00 0.44 ± 0.01

0.00 ± 0.00 0.10 ± 0.01 0.00 ± 0.00 0.09 ± 0.00 0.75 ± 0.02

0.00 ± 0.00 0.13 ± 0.01 0.00 ± 0.00 0.07 ± 0.01 0.45 ± 0.01

0.00 ± 0.00 0.08 ± 0.00 0.00 ± 0.00 0.11 ± 0.01 0.75 ± 0.01

0.00 ± 0.00 0.00 ± 0.00 0.10 ± 0.00 0.07 ± 0.01 0.61 ± 0.03

0.00 ± 0.00 0.11 ± 0.01 0.00 ± 0.00 0.10 ± 0.00 0.48 ± 0.00

0.00 ± 0.00 0.00 ± 0.00 0.10 ± 0.01 0.08 ± 0.00 0.66 ± 0.01

0.00 ± 0.00 0.14 ± 0.01 0.00 ± 0.00 0.11 ± 0.01 0.72 ± 0.00

0.00 ± 0.00 0.00 ± 0.00 0.13 ± 0.01 0.09 ± 0.01 0.88 ± 0.02

0.00 ± 0.00 0.00 ± 0.00 0.08 ± 0.01 0.06 ± 0.00 0.69 ± 0.03

MS RI, MS RI, MS STD, MS STD, MS

0.28 ± 0.02

0.23 ± 0.05

0.55 ± 0.01

1.03 ± 0.01

0.75 ± 0.01

0.77 ± 0.00

0.07 ± 0.02

0.60 ± 0.00

0.07 ± 0.01

0.71 ± 0.02

0.06 ± 0.01

0.04 ± 0.01

STD, MS

0.23 ± 0.01 3.39 ± 0.05 0.08 ± 0.00

0.27 ± 0.00 3.93 ± 0.05 0.11 ± 0.01

0.19 ± 0.00 1.58 ± 0.01 0.22 ± 0.00

0.17 ± 0.00 2.47 ± 0.04 0.16 ± 0.01

0.22 ± 0.00 2.36 ± 0.02 0.22 ± 0.02

0.19 ± 0.00 3.25 ± 0.02 0.18 ± 0.00

0.19 ± 0.01 1.40 ± 0.02 0.00 ± 0.00

0.22 ± 0.00 1.83 ± 0.03 0.18 ± 0.01

0.07 ± 0.00 1.91 ± 0.02 0.00 ± 0.00

0.21 ± 0.00 1.76 ± 0.01 0.23 ± 0.00

0.13 ± 0.01 2.40 ± 0.02 0.00 ± 0.00

0.17 ± 0.01 1.69 ± 0.04 0.00 ± 0.00

RI, MS STD, MS RI, MS

2.30 ± 0.03 0.17 ± 0.02 0.93 ± 0.01 1.42 ± 0.04 49.46 ± 1.05

1.18 ± 0.01 0.33 ± 0.01 1.39 ± 0.01 0.94 ± 0.01 27.72 ± 0.40

1.39 ± 0.02 0.18 ± 0.00 0.85 ± 0.01 1.34 ± 0.01 50.05 ± 0.33

1.32 ± 0.03 0.13 ± 0.00 0.53 ± 0.02 1.76 ± 0.05 52.22 ± 0.83

1.78 ± 0.02 0.18 ± 0.01 0.56 ± 0.01 1.40 ± 0.03 49.21 ± 0.30

1.47 ± 0.02 0.16 ± 0.01 0.68 ± 0.01 2.47 ± 0.04 55.24 ± 0.38

0.42 ± 0.05 0.32 ± 0.02 2.27 ± 0.05 1.17 ± 0.04 58.65 ± 0.86

1.32 ± 0.02 0.19 ± 0.01 0.69 ± 0.01 1.41 ± 0.01 49.94 ± 0.44

0.12 ± 0.10 0.31 ± 0.02 2.67 ± 0.11 1.01 ± 0.01 48.73 ± 0.44

1.49 ± 0.02 0.20 ± 0.01 1.00 ± 0.02 1.50 ± 0.02 52.81 ± 0.40

0.59 ± 0.01 0.44 ± 0.01 3.63 ± 0.11 1.11 ± 0.03 45.83 ± 1.29

0.39 ± 0.03 0.28 ± 0.01 3.08 ± 0.05 1.15 ± 0.03 57.72 ± 1.24

RI, MS RI, MS STD, MS STD, MS RI, MS

0.43 ± 0.01

0.63 ± 0.02

0.62 ± 0.04

0.43 ± 0.04

0.46 ± 0.04

0.61 ± 0.00

0.80 ± 0.03

0.53 ± 0.02

0.00 ± 0.00

0.59 ± 0.02

0.58 ± 0.06

0.98 ± 0.04

RI, MS

STD, MS = confirmed by injection of standard and by mass spectra library; RI, MS = confirmed by n-alkanes retention index by mass spectra library; MS = tentative identification = confirmation only by mass spectra library. Results are the mean of three replications ± S.D. P < 0.05. D25, D50 and D75: sole cropping of dill at 25, 50 and 75 plants m−2 , respectively. D/C: dill/common bean intercropping. +AM, −AM: with and without arbuscular mycorrhiza colonization, respectively.

W. Weisany et al. / Industrial Crops and Products 77 (2015) 295–306

Compounds (synonymous)

W. Weisany et al. / Industrial Crops and Products 77 (2015) 295–306

301

Fig. 3. Land equivalent ratio (LER) of common bean and dill inoculated (M) and non-inoculated (non-m) with arbuscular mycorrhiza (Funneliformis mosseae) in 2013 and 2014. Results are the mean of three replications ± SD. P < 0.05. D/C: The additive intercropping of dill + common bean (25 + 40, 50 + 40 and 75 + 40 plants m−2 ).

(D25 + C40), compared to sole cropping (C40) (Table 3). However, there was no significant difference between plants under D75 + C40 and D50 + C40 cropping systems. Chlorophyll content in dill and common bean leaf were also affected by inoculation with AM (P ≤ 0.001) (Table 3). In general, intercropped plants inoculated with AM produced significantly more chlorophyll in comparison with non-inoculated plants in 2013 and 2014.

3.5. Land equivalent ratio Except for D75 + C40 cropping system at non-inoculated with AM plants in 2013 for common bean and 2014 for dill, the partial LER values were greater than 1 (Fig. 2a and b), which suggests an overall yield advantage of intercrops relative to sole crops. AM colonization significantly increased LER in both 2013 and 2014. The highest LER (3.37) was obtained from dill with common bean intercrop (D25 + C40) and AM colonization in 2014 and the lowest (1.73) in dill with common bean (D75 + C40) and non-inoculated plants in 2013 (Fig. 3).

3.6. Essential oil yield Essential oil yield was significantly influenced by cropping systems. In 2014, intercropping of dill with common bean (D50 + C40) increased EO yield of shoot in dill compared to sole cropping (D25 and D50) (Fig. 4). However, there was no significant difference between other levels of sole and intercropping systems in terms of EO yield. AM colonization markedly increased EO yield of dill shoot in 2013 and 2014 (Fig. 5). Analyzing the chemical composition of EO, dill apiole was the main component in all treatments and its content varied among the treatments (Table 4, Figs. 6 and 7). The second main component of the EO was dill ether, with contents varying from 16.49 to 24.26% (Table 4). In intercropped plants (D70 + C40) inoculated with F. mosseae, the ␣-phellandrene, limonene, ␤-phellandrene, terpinen4-ol, cryptone and carvone content in EO increased to 12.68, 6.83, 3.12, 0.23, 0.27 and 3.93%, respectively (Table 4). Also, AM colonization significantly increased iso-dihydrocarvone, myristicin and apiole in both sole and intercropping systems. However, in sole competed plants inoculated with AM, the ␣-terpinene, p-cymene,

Fig. 4. Essential oil yield at different cropping systems in 2013 and 2014. Results are the mean of three replications ± SD. P < 0.05. D25, D50 and D75: sole cropping of dill at 25, 50 and 75 plants m−2 , respectively. DC: dill + common bean intercropping.

302

W. Weisany et al. / Industrial Crops and Products 77 (2015) 295–306

Fig. 5. Essential oil yield of dill shoot inoculated and non-inoculated with arbuscular mycorrhiza (AM) (Funneliformis mosseae) in 2013 and 2014. Results are the mean of three replications ± SD. P < 0.05.

␣-terpinolene, p-˛-dimethylstyrene, dill ether, n-dihydrocarvone and cis-sabinol content in EO decreased (Table 4, Figs. 6 and 7).

4. Discussion Intercropping of common bean and dill increased fresh weight to a large extent compared to sole cropping during the two years. The intercropped plants produced more yield per unit area than both sole crops, which indicates that intercropping is more profitable than sowing a single crop (LER greater than one) (Vandermeer, 1989). Yielding observed in intercrops could be partly explained by resource use complementarity in time and space between different crops within intercrops (Caviglia and Sadras, 2004). Besides, legume crops such as common bean, thanks to symbiotic fixation of atmospheric nitrogen, may alleviate soil nitrogen restrictions of accompanying non-legume crops, which may consequently improve the overall productivity (Vandermeer, 1989). Furthermore, this advantage is probably the result of different above and below-ground growth habits and the morphological characteristics of the intercrop components, allowing their more efficient utilization of plant growth resources, i.e., water, nutrients, and radiant energy (Fukai and Trenbath, 1993). Dill fresh weight was affected by AM colonization and different cropping systems. Previous our studies have shown that different species and isolates of Glomus increased plant height, total dry weight and root and shoot dry weights of chickpea (Sohrabi et al., 2012a,b). Studying oregano and mint, Karagiannidis et al. (2011) it was found that the dry mass of AM inoculated plants increased from 2 to 4.7 fold when compared with non-inoculated plants. The same was observed by Khaosaad et al. (2006). The high efficiency of the intercropping systems found in this study as supported by higher total LER is in agreement with the findings of Baumann et al. (2001), who attributed this phenomenon to the complementary use of resources in plant production allowing an interspecific facilitation. LUE was previously reported to be higher in intercrops than monocultures (Yang et al., 2011; Agegnehu et al., 2006). Hauggaard-Nielsen et al. (2003) had reported that the calculated LER proved that plant growth resources were used from 27 to 31% more efficiently by intercrop than the sole crop. In this study LER was increased by AM colonization. This facilitation plant phenomenon (Callaway et al., 1991) has been attributed to leguminous species because of their symbiotic interactions which lead to production of nutrient rich litter, also to

the ability of mycorrhizal hyphae to decompose organic matter (Scotti and Correa, 2004) and improve soil nutrient availability (Smith and Read, 2008). Moreover, it has been proven that the more active mechanism involved is the AM transfer (Francis et al., 1986; Haystead et al., 1988). Guzmán-Plazola et al. (1992) confirmed under field conditions that natural mycorrhizal links are established in intercrops between maize and bean. Our previous studies have shown that different species and isolates of Glomus spp. had diverse effects on mycorrhized plants (Sohrabi et al., 2012a,b). In both sole and intercropping systems, the chlorophyll content and fresh weight were higher in mycorrhized plants than in non mycorrhized plants. AM fungi by improving nutrition (McArthur and Knowles, 1993), can enhance chlorophyll content (Rachel et al., 1992). These results are in agreement with those previously found by Mathur and Vyas (2000). They detected that AM root colonization increased chlorophyll synthesis. The association of AM fungi with the roots of common bean and dill plants influence Mg, Cu, Zn, Fe and Mn acquisition that have poor mobility rates. Also, zinc is essential component of chlorophyll molecule and chlorophyll protein (Wiedenhoeft, 2006). Intercropping system increased zinc content of shoot in common bean and dill (data not presented). Thus, the enhancement in photosynthetic pigments content observed in the present study may be attributed to increased contents of Zn in leaves of intercropped plantlets in comparison to the sole cropped plantlets. Improved growth and survivability of mycorrhizal A. graveolens L. plantlets in this study may be due to an increase in chlorophyll content in their leaves. Intercropping increased EO yield of dill shoot. Our results are in agreement with those of Maffei and Mucciarelli (2003), who noted that intercropped peppermint plants produced a significantly higher amount of EO when compared to sole cropped plants, and the EO yield had increased. Inoculation dill with AM resulted in yield and quality increases in the EO compared to non-inoculated dill plants. The effectiveness of AM fungi in increasing the production of EO has been demonstrated in several aromatic plant species (Gupta et al., 2002; Kapoor et al., 2002a,b, 2007; Khaosaad et al., 2006; Freitas et al., 2004; Copetta et al., 2006; Chaudhary et al., 2008). The same response was found by Karagiannidis et al. (2011) in their study of three AM fungi isolated inoculation that increased the growth, nutrient content and EO yield of oregano and mint plants. The increased EO production is result of the increased production of shoot fresh matter (Subrahmanyam et al., 1992; Piccaglia et al., 1993). AM fungi promote the absorption of phosphorous

W. Weisany et al. / Industrial Crops and Products 77 (2015) 295–306

303

Fig. 6. Anethum graveolens essential oil chromatogram carried out using a gas chromatograph mass spectrometry. Essential oils were obtained from non-inoculated with arbuscular mycorrhiza (Funneliformis mosseae) and sole and intercropped plants.

by plants (data not shown). P nutrition may play a direct role in increasing the contents of secondary metabolites (Abu-Zeyad et al., 1999). Kapoor et al. (2004) obtained similar results for the accumulation of EO in fennel. Moreover, Copetta et al. (2006) found that G. rosea increased EO yield was associated to a significantly larger number of peltate glandular trichomes (main sites of EO synthesis and accumulation) in the leaves of inoculated plants. They suggested that the greater number of trichomes could be related to alterations in the phytohormonal profile induced by AM fungi (Copetta et al., 2006). Furthermore, in the studies by Kapoor et al. (2007), AM were found to increase the number of glandular trichomes of A. annua L. and, as a consequence, enhance the content of artemisinin in leaves. A significant increase was noticed in ␣-phellandrene, limonene, ␤-phellandrene, terpinen-4-ol, cryptone and carvone content of intercropped plants, whereas ␣-terpinene, p-cymene, ␣terpinolene, p-␣-dimethylstyrene, dill ether, n-dihydrocarvone and cis-sabinol significantly decreased content of sole cropped plants. Changes in the essential oil composition as response to cropping system was also observed by Maffei and Mucciarelli (2003). They indicated, intercropped plants showed a significantly higher content of most of the main oil components with the exception of minor components such as g-terpinene, Z-ocimene, p-cymene, neomenthola-terpineol, germacrene D and piperitone. In contrast,

the chemical profile of the aromatic oil was not influenced either by cropping systems (Maffei and Mucciarelli, 2003). In our results, changes in EO composition were found following AM colonization. The content of ␣-phellandrene, limonene, ␤-phellandrene, terpinen-4-ol, cryptone, carvone, iso-dihydrocarvone, myristicin and apiole was enhanced whit AM colonozition. These findings are in agreement with those of Kapoor et al. (2002b). They indicated that inoculation with AM fungi increased the total EO content of Coriandrum sativum, especially geranial and linalool. Moreover, Karagiannidis et al. (2011) in mint plants, concluded that mycorrhizal plants had relatively high levels of limonene, 1,8-cineole, carvone, eugenol and (e)-methyl cinnamate. Furthermore, Geneva et al. (2010) observed that AM formation in Salvia officinalis changes the composition of EO, and promotes the relative quantities of bornylacetate, 1,8-cineole, ␣-thujones and ␤-thujones. The mechanism behind changes in EO composition is not known and it is possible that it may be related to better nutrition. However, Khaosaad et al. (2006) concluded that the quantitative increase in oregano EO with AM was not due to improved P nutrition. Whereas, AM colonization increased iso-dihydrocarvone, myristicin and apiole content, the content of ␣-terpinene, p-cymene, ␣-terpinolene, p-␣-dimethylstyrene, dill ether, ndihydrocarvone and cis-sabinol in EO was decreased in inoculated plants with AM (Figs. 6 and 7). Similarly, AM symbiosis significantly

304

W. Weisany et al. / Industrial Crops and Products 77 (2015) 295–306

Fig. 7. Anethum graveolens essential oil chromatogram carried out using a gas chromatograph mass spectrometry. Essential oils were obtained from inoculated with arbuscular mycorrhiza (Funneliformis mosseae) and sole and intercropped plants.

increases the contents of not only the EO but also the important active ingredient anethol in fennel (F. vulgare) (Kapoor et al., 2004). In contrast, Khaosaad et al. (2006) found that root colonization of oregano plants by F. mosseae did not affect significantly the composition of EO. Most likely these changes are due to changes in the synthesis pathways, and the role of these EO play in plant physiology. 5. Conclusion The findings of the present study suggest that intercropping of common bean and dill with AM coloniziton is a way to increase productivity per unit area. AM colonization and intercropping with common bean increased fresh weight, chlorophyll content and LER compared to non-AM colonization and sole cropping system. When plant species are intercropped with AM colonization, it is likely that yield advantages occur as a result of complementary use of resources by the crops. A. graveolens L. EO yield was increased in AM colonization and intercropping systems. AM colonization increased iso-dihydrocarvone, myristicin and apiole content in both sole and intercropping systems. Moreover, intercropping system and AM fungi influenced the production of carvone, myristicin and apiole content in dill EO composition. These composition are very important in industrial uses such as potato sprout inhibitor and natural pesticides. Hence, it was concluded that intercropping system and AM colonization should be employed to help in the reduction of fertilizer, pesticides and other agrochemical inputs, thus

enhancing the sustainability of the commercial cultivation of medicinal plants. Acknowledgements This research was supported by the University of Tabriz. We would also like to thank Fondazione Edmund Mach di San Michele all’Adige for technical support. We thank Dr. Urska Vrhovsek and Cesare Lotti for useful discussions. References Abu-Zeyad, R., Khan, A.G., Khoo, C., 1999. Occurrence of arbuscular mycorrhiza in Castanospermum austral A. Cunn, C. Fraser and effects on growth and production of castanospermine. Mycorrhiza 9, 111–117. Adam, R.P., 2008. Identification of Essential Oil Components by Gas Chromatography/Mass Spectrometry. Allured Publishing Corporation. Adams, R.P., Habte, M., Park, S., Dafforn, M.R., 2004. Preliminary comparison of vetiver root essential oils from cleansed (bacteria- and fungus-free) versus non-cleansed (normal) vetiver plants. Biochem. Syst. Ecol. 32, 1137–1144. Agegnehu, G., Ghizaw, A., Sinebo, W., 2006. Yield performance and land-use efficiency of barley and faba bean mixed cropping in Ethiopian highlands. Eur. J. Agron. 25, 202–207. Akiyama, K., Hayashi, H., 2002. Arbuscular mycorrhizal fungus- promoted accumulation of two new triterpenoids in cucumber roots. Biosci. Biotechnol. Biochem. 66, 762–769. Anil, L., Park, J., Phipps, R.H., Miller, F.A., 1998. Temperate intercropping of cereals for forage: a review of the potential for growth and utilization with particular reference to the UK. Grass Forage Sci. 53, 301–317. Barrios, E., 2007. Soil biota, ecosystem services and land productivity. Ecol. Econ. 64, 269–285.

W. Weisany et al. / Industrial Crops and Products 77 (2015) 295–306 Baumann, D.T., Bastiaans, L., Kropff, M.J., 2001. Competition and rop performance in a leek-celery intercropping system. Crop Sci. 41, 764–774. Callaway, R.M., Nadkarni, N.M., Mahall, B.E., 1991. Facilitation and interference of Quercus douglasiion understory productivity in Central California. Ecology 72, 1484–1499. Caviglia, O.P., Sadras, V.O., 2004. Long-term simulation of productivity in crop sequences differing in intensification in the Argentina pampas. In: Proceedings of the 4th International Crop Science Congress, Brisbane, Australia, 26 September–1 October. Chaudhary, V., Kapoor, R., Bhatnagar, A.K., 2008. Effectiveness of two arbuscular mycorrhizal fungi on concentrations of essential oil and artemisinin in three accessions of Artemisia annua L. Appl. Soil Ecol. 40, 174–181. Copetta, A., Lingua, G., Berta, G., 2006. Effects of three AM fungi on growth, distribution of glandular hairs, and essential oil production in Ocimum basilicum L. var: Genovese. Mycorrhiza 16, 485–494. Devi, M.C., Reddy, M.N., 2002. Phenolic acid metabolism of groundnut (Arachis hypogaea L.) plants inoculated with VAM fungus and Rhizobium. Plant Growth Regul. 37, 151–156. Duke, J.A., 2001. Handbook of Medicinal Herbs. CRC Press LLC, USA, pp. 42–$9. Farag, R.S., Daw, Z.Y., Abo-Raya, S.H., 1989. Influence of some spice essential oils on Aspetgihs parasiticus and production of aflatoxins in a synthetic medium. J. Food Sci. 54, 14–76. Fester, T., Hause, B., Schmidt, D., Halfmann, K., Schmidt, J., Wray, V., Hause, G., Strack, D., 2002. Occurrence and localization of apocarotenoids in arbuscular mycorrhizal plant roots. Plant Cell Physiol. 43, 256–265. Francis, R., Finlay, R.D., Read, D.J., 1986. Vesicular-arbuscular mycorrhiza in natural vegetation systems. IV. Transfer of nutrients in inter- and intra-specific combinations of host plants. New Phytol. 102, 103–111. Freitas, M.S.M., Martins, M.A., Curcino Vieira, I.J., 2004. Yield and quality of essential of Mentha arvensis in response to inoculation with arbuscular mycorrhizal fungi. Pesqui. Agropecu. Bras. 39, 887–894. Fukai, S., Trenbath, B.R., 1993. Processes determining intercrop productivity and yields of component crops. Field Crops Res. 34, 247–271. Geneva, M.P., Stancheva, I.V., Boychinova, M.M., Mincheva, N.H., Yonova, P.A., 2010. Effects of foliar fertilization and arbuscular mycorrhizal colonization on Salvia officinalis L. growth, antioxidant capacity, and essential oil composition. J. Sci. Food Agric. 90, 696–702. Ghosh, P.K., 2004. Growth, yield, competition and economics of groundnut/cereal fodder intercropping systems in the semi-arid tropics of India. Field Crops Res. 88, 227–237. Gupta, M.L., Prasad, A., Ram, M., Kumar, S., 2002. Effect of the vesicular arbuscular mycorrhizal (VAM) fungus Glomus fasciculatum on the essential oil yield related characters and nutrient acquisition in the crops of different cultivars of menthol mint (Mentha arvensis) under field conditions. Bioresour. Technol. 81, 77–79. Guzmán-Plazola, R.A., Ferrera-Cerrato, R., Bethlenfalvay, G.J., 1992. Papel de la endomicorrhiza V-A en la transferencia de exudados radicales entre frijol y maíz sembrados en asociación bajo condiciones de campo. Terra 10, 236–248. Hartmans, K.J., Diepenhorts, P., Bakker, W., Gorris, L.G.M., 1995. The use of carvone in agriculture: sprout suppression of potatoes and antifungal activity against potato tuber and other plant diseases. Ind. Crop Prod. 4, 3–13. Hauggaard-Nielsen, H., Ambus, P., Jensen, E.S., 2003. The comparison of nitrogen use and leaching in sole cropped versus intercropped pea and barley. Nutr. Cycl. Agroecosyst. 65 (3), 289–300. Haystead, S., Malajczvk, N., Grove, T.S., 1988. Underground transfer of nitrogen between pasture plants infected with vesicular-arbuscular mycorrhizal fungi. New Phytol. 108, 417–423. Jeffries, P., Gianinazzi, S., Perotto, S., Turnau, K., Barea, J.M., 2003. The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol. Fertil. Soils 37, 1–16. Kapoor, R., Giri, B., Mukerji, K.G., 2002a. Glomus macrocarpum: a potential bioinoculant to improve essential oil quality and concentration in Dill (Anethum graveolens L.) and Carum (Trachyspermum ammi (Linn.) Sprague). World J. Microbiol. Biotech. 18, 459–463. Kapoor, R., Giri, B., Mukerji, K.G., 2002b. Mycorrhization of coriander (Coriandrum sativum L.) to enhance the concentration and quality of essential oil. J. Sci. Food Agric. 82, 339–342. Kapoor, R., Giri, B., Mukerji, K.G., 2004. Improved growth and essential oil yield and quality in Foeniculum vulgare mill on mycorrhizal inoculation supplemented with P-fertilizer. Bioresour. Technol. 93, 307–311. Kapoor, R., Chaudhary, V., Bhatnagar, A.K., 2007. Effects of arbuscular and phosphorus application on artemisinin concentration in Artemisia annua L. Mycorrhiza 17, 581–587. Karagiannidis, N., Thomidis, T., Lazari, D., Panou-Filotheou, E., Karagiannidou, C., 2011. Effect of three Greek arbuscular mycorrhizal fungi in improving the growth nutrient concentration, and production of essential oils of oregano and mint plants. Sci. Hortic. 129, 329–334. Khaosaad, T., Vierheilig, H., Ziltterl-Egleer, K., Novak, J., 2006. Arbuscular mycorrhiza alters the concentration of essential oils in oregano (Origanum sp., Lamiaceae). Mycorrhiza 16, 443–446. Larose, G., Chenevert, R., Moutoglis, P., Gagne, S., Piché, Y., Vierheilig, H., 2002. Flavonoid levels in roots of Medicago sativa are modulated by the developmental stage of the symbiosis and the root colonizing arbuscular mycorrhizal fungus. J. Plant Physiol. 159, 1329–1339.

305

Li, L., Tang, C., Rengel, Z., Zhang, S., 2004. Calcium, magnesium and micro-element uptake as affected by phosphorus sources and interspecific root interactions between wheat and chickpea. Plant Soil 261, 29–37. Maffei, M., Mucciarelli, M., 2003. Essential oil yield in peppermint/soybean strip intercropping. Field Crops Res. 84, 229–240. Mathur, N., Vyas, A., 2000. Influence of arbuscular mycorrhizae on biomass production, nutrient uptake and physiological changes in Ziziphus mauritana Lam. under water stress. J. Arid Environ. 45, 191–195. McArthur, D.A.J., Knowles, N.R., 1993. Influence of VAM fungi and nutrition on growth development, and mineral nutrition of potato. Plant Physiol. 102, 771–782. McGonigle, T.P., Miller, M.H., Evans, D.G., Fairchild, D.L., Swan, G.A., 1990. A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol. 115, 495–501. Mead, R., Willey, R.W., 1980. The concept of a land equivalent ratio and advantages in yields from intercropping. Exp. Agric. 16, 217–228. Morelli, I., 1981. I Principi Attivi Delle Piante Medicinali. Edagricole, Bologna, Italy (in Italian). Mucciarelli, M., Scannerini, S., Bertea, C., Maffei, M., 2003. In vitro and in vivo peppermint (Mentha piperita) growth promotion by nonmycorrhizal fungal colonization. New Phytol. 158, 579–591. Nell, M., Wawrosch, C., Steinkellner, S., Vierheilig, H., Kopp, B., Lossi, A., 2010. Root colonization by symbiotic Arbuscular mycorrhizal fungi increases sesquiterpenic acid concentrations in Valeriana officinalis L. Planta Med. 76, 393–398. Piccaglia, R., Dellacecca, V., Marotti, M., Giovanelli, E., 1993. Agronomic factors affecting the yields and the essential oil composition of peppermint (Mentha piperita L.). Acta Hortic. 344, 29–40. Rachel, E.K., Reddy, S.R., Reddy, S.M., 1992. Seedling preinoculation within AM fungi on transplant survival and growth of sunflower. Proc. Natl. Acad. Sci. India B 62, 429–432. Rajeshkumar, S., Nisha, M.C., Selvaraj, T., 2008. Variability in growth, nutrition and phytochemical constituents of Plectranthus amboinicus (Lour) Spreng. As influenced by indigenous arbuscular mycorrhizal fungi. Maejo Int. J. Sci. Technol. 2, 431–439. Rapparini, F., Llusià, J., Penuelas, J., 2008. Effect of arbuscular mycorrhizal (AM) colonization on terpene emission and content of Artemisia annua L. Plant Biol. 10, 108–122. Rasouli-Sadaghianil, M.H., Hassani, A., Barin, M., Danesh, Y.R., Sefidkon, F., 2010. Effects of arbuscular mycorrhizal (AM) fungi on growth, essential oil production and nutrients uptake in basil. J. Med. Plants Res. 4 (21), 2222–2228. Rojas-Andrade, R., Cerda-Garcia-Rojas, C.M., Frias-Hernandez, J.T., Dendooven, L., Olalde-Portugal, V., Ramos-Valdivia, A.C., 2003. Changes in the concentration of trigonelline in a semi-arid leguminous plant (Prosopis laevigata) induced by an arbuscular mycorrhizal fungus during the presymbiotic phase. Mycorrhiza 13, 49–52. Scotti, M.R.M., Correa, E.J.A., 2004. Growth and litter decomposition of woody species inoculated with rhizobia and arbuscular mycorrhizal fungi in semiarid Brazil. Ann. Sci. 61, 87–95. Smith, S.E., Read, D., 2008. Mycorrhizal Symbiosis. Acad. Press, London, UK. Sohrabi, Y., Heidari, G., Weisany, W., Ghasemi Golezani, K., Mohammadi, K., 2012a. Some physiological responses of chickpea (Cicer aritinum L.) cultivars to arbuscular mycorrhiza under drought stress. Russ. J. Plant Physiol. 59 (6), 708–716. Sohrabi, Y., Heidari, G., Weisany, W., Ghasemi Golezani, K., Mohammadi, K., 2012b. Changes of antioxidativ eenzymes, lipid peroxidation and chlorophyll content in chickpea types colonized by different Glomus species under drought stress. Symbiosis 56, 5–18. Songa, J.M., Jiang, N., Schulthess, F., Omwega, C., 2007. The role of intercropping different cereal species in controlling lepidopteran stemborers on maize in Kenya. J. Appl. Entomol. 131, 40–49. Su, H.C.F., 1985. Laboratory study on effects of Anethum graveolens seed on four species of stored-product insects. J. Econ. Entomol. 78, 451–453. Subrahmanyam, K., Nair, A.K., Chattopadhyay, A., Singh, D.V., 1992. Evaluation of ammonium polyphosphate as phosphorus source in Japanese mint (Mentha arvensis subsp. haplocalyx var piperascens). Indian J. Agric. Sci. 62, 554–556. Vandermeer, J., 1989. The Ecology of Intercropping. Cambridge University Press, Cambridge, UK. Vierheilig, H., Bennett, R., Kiddle, G., Kaldorf, M., Ludwig-Müller, J., 2000a. Differences in glucosinolate patterns and arbuscular mycorrhizal status of glucosinolate-containing plant species. New Phytol. 146, 343–352. Vierheilig, H., Gagnon, H., Strack, D., Maier, W., 2000b. Accumulation of cyclohexenone derivatives in barley, wheat and maize roots in response to inoculation with different arbuscular mycorrhizal fungi. Mycorrhiza 9, 291–293. Vierheilig, H., Maier, W., Wyss, U., Samson, J., Strack, D., Piché, Y., 2000c. Cyclohexenone derivative- and phosphate-levels in split-root systems and their role in the systemic suppression of mycorrhization in precolonized barley plants. J. Plant Physiol. 157, 593–599. Vierheilig, H., Schweiger, P., Brundrett, M., 2005. An overview of methods for the detection and observation of arbuscular mycorrhizal fungi in roots. Physiol. Plant 125, 393–404. Vokou, D., Vareltzidou, S., Katinakis, P., 1993. Effects of aromatic plants on potato storage: sprout suppression and antimicrobial activity. Agric. Ecosyst. Environ. 47, 223–235.

306

W. Weisany et al. / Industrial Crops and Products 77 (2015) 295–306

Volpin, H., Eelkind, Y., Okon, Y., Kapulnik, Y., 1994. A vesicular arbuscular mycorrhizal fungus (Glomus intraradix) induces a defense response in alfafa roots. Plant Physiol. 104, 683–689. Wiedenhoeft, A.C., 2006. Plant Nutrition. Chelsea Publisher, New York. Wondimu, T., Afar, Z., Kelbessa, E., 2007. Ethnobotanical study of medicinal plants around ‘Dheeraa’ town, Arsi Zone, Ethiopia. J. Ethnopharmacol. 112, 152–161. Yang, C.H., Huang, G.B., Chai, Q., Luo, Z.X., 2011. Water use and yield of wheat/maize intercropping under alternate irrigation in the Oasis field of northwest China. Field Crops Res. 124, 426–432.

Yao, M.K., Désilets, H., Charles, M.T., Boulanger, R., Tweddell, R.J., 2003. Effect of mycorrhization on the accumulation of rhishitin and solavetivone in potato plantlets challenged with Rhizoctonia solani. Mycorrhiza 13, 333–336. Zhang, F., Li, L., 2003. Using competitive and facilitative interactions in inter-cropping systems enhances crop productivity and nutrient-use efficiency. Plant Soil 248, 305–312. Zuo, Y.M., Li, X., Cao, Y.P., Zhang, F.S., Christie, P., 2003. Iron nutrition of pea-nut enhanced by mixed cropping with maize: possible role of root morphology and rhizosphere microflora. J. Plant Nutr. 26, 2093–2110.