Photochemical response of parsley (Petroselinum crispum (Mill.) Fuss) grown under red light: The effect on the essential oil composition and yield

Photochemical response of parsley (Petroselinum crispum (Mill.) Fuss) grown under red light: The effect on the essential oil composition and yield

Accepted Manuscript Photochemical response of parsley (Petroselinum crispum (Mill.) Fuss) grown under red light: The effect on the essential oil compo...

NAN Sizes 1 Downloads 15 Views

Accepted Manuscript Photochemical response of parsley (Petroselinum crispum (Mill.) Fuss) grown under red light: The effect on the essential oil composition and yield

Roberta Ascrizzi, Daniele Fraternale, Guido Flamini PII: DOI: Reference:

S1011-1344(18)30298-7 doi:10.1016/j.jphotobiol.2018.06.006 JPB 11272

To appear in:

Journal of Photochemistry & Photobiology, B: Biology

Received date: Revised date: Accepted date:

19 March 2018 25 May 2018 20 June 2018

Please cite this article as: Roberta Ascrizzi, Daniele Fraternale, Guido Flamini , Photochemical response of parsley (Petroselinum crispum (Mill.) Fuss) grown under red light: The effect on the essential oil composition and yield. Jpb (2018), doi:10.1016/ j.jphotobiol.2018.06.006

This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

ACCEPTED MANUSCRIPT Photochemical response of parsley (Petroselinum crispum (Mill.) Fuss) grown under red light: The effect on the essential oil composition and yield

PT

Roberta Ascrizzi1,*, Daniele Fraternale2, Guido Flamini1 Department of Pharmacy, University of Pisa, Via Bonanno 6, 56126 Pisa, Italy

2

Department of Biomolecular Sciences, Plant Biology Section, University of Urbino Carlo Bo, Via

SC

RI

1

NU

Bramante 28, 61029 Urbino (PU), Italy

AC

CE

PT E

D

MA

*Corresponding author. E-mail address: [email protected]

ACCEPTED MANUSCRIPT

Abstract The effect of different wavelengths on plants morphological characters has been widely described, but also the chemical composition of the essential oil is influenced by the lighting conditions in which

PT

they are grown. In the present study, the effect of both the enrichment (reverse Emerson effect) and the monochromatic lighting treatments with red light has been evaluated on the essential oil

RI

compositions of parsley (Petroselinum crispum (Mill.) Fuss). Multivariate statistical analysis was

SC

performed on the results, with both the hierarchical cluster and principal component analyses. Whilst the red-enrichment of the light spectrum did not induce major changes in the essential oil

NU

composition, the end of the day monochromatic red (660 nm) treatment caused a chemotype switch

MA

in the essential oil and relevant differences in the overall composition, with an increment of the relative abundance of oxygenated compounds, coupled with a relevant decrement in the abundance

D

of phenylpropanoids. The extraction yields remained unchanged in all the three tested conditions of

PT E

light (control, red-enriched and monochromatic red). Different lighting conditions could be used as a tool to modulate the compounds present in the essential oil, but further studies would be advisable to

CE

assess the effects on different species and chemical classes of compounds.

AC

Keywords Petroselinum crispum; red wavelength; light; essential oil; change of chemotype

ACCEPTED MANUSCRIPT 1. Introduction Photomorphogenic responses to different lighting condition in plants growth are widely studied, ranging from experiments with different fluorescent or LED lamps or with the aid of colored nets. Warrington and Mitchell (1976) studied the effect of different lights on several crop plants, reporting that red lighting produced taller and straighter plants, with thinner but longer and wider leaves, in

PT

which the carbohydrates content is higher. Nishioka et al. (2008), as well, reported a red light-induced

RI

enhancement in Japanese mint samples growth, with the expansion of both leaf area and width.

SC

Noguchi and Amaki (2011) confirmed the morphological response of leaves to red light: Mexican mint plants produce thicker and narrower leaves under blue light, whilst they result thinner and wider

NU

under the red light. Mulas et al. (2006) also reported an increased height of Rosmarinus officinalis plants grown under red light (660 nm). The photochemical response to different light treatment in

MA

plants has been studied for in vitro growth as well: Batista et al. (2016) reported the influence of blue and red light on the composition of the essential oil hydrodistilled from in vitro grown Lippia alba.

D

The effect of red lighting conditions on plant volatiles has also been studied in the head-space

PT E

emission: Noguchi and Amaki (2011) analyzed the spontaneous head-space emission profile in Mexican mint plants. Their head-space analyses show a completely different behavior of the chemical

CE

classes of compounds: shorter retention times compounds (like monoterpenes) were more abundant

AC

in the headspace of plants grown under red lighting conditions, whilst it is the opposite in the essential oil in the present study.

The enrichment of longer wavelengths with shorter wavelengths lighting is known as Emerson addition effect: the photosynthetic efficiency of monochromatic light, indeed, drops rapidly at wavelengths longer than 685 nm but can be improved with the addition of shorter wavelengths [6]. In the present study, we analysed the reverse Emerson effect, namely the addition of longer wavelengths (red light) to a warm-white light: this condition is far less studied than the previous one, and, to the best of our knowledge, there are no other published reports on the photochemical response

ACCEPTED MANUSCRIPT of P. crispum to this lighting treatment. Zhen and van Iersel (2017) report the photomorphological response to longer (red and far-red) wavelengths-enriched light treatments of Lactuca sativa ‘Green Towers’: far-red photons reduce the dissipation of the absorbed light as heat and, like the red photons (600-680 nm), increase the photosynthetic efficiency. In the present study, the effect of red light-enrichment and red light treatments on Petroselinum

PT

crispum essential oil composition have been studied. To the best of our knowledge, no other studies

RI

have been published reporting the effect of these modified light conditions on essential oil production

SC

for P. crispum.

NU

2. Materials and methods 2.1. Plant material and growth conditions

MA

The seeds of Petroselinum crispum (Mill.) Fuss were purchased from Fioral srl, Cesena (FC), Italy, lot number YG0016, and were seeded in three pots (diameter: 36 cm, height 16 cm) filled with a

D

mixture of commercial substrate (Compo-Italy) consisting of 20% vermiculite and 80% of the land

PT E

for vegetable garden. In each pot, 40 grams of parsley seeds were uniformly seeded. Throughout the cultivation, the land of the three pots was watered with the same amount of water. The methodology

CE

consisted in the investigation of the influence of red light on the chemical composition of the essential oil of parsley. The control sample was placed in a climatic chamber at 25±2°C and subjected to a 16

AC

hours photoperiod provided only with fluorescent tubes Fluora-OSRAM at light intensity of 60 μmol m-2 s-1. The red-enriched sample was subjected to a 16 hours photoperiod always in the climatic chamber as above (with Fluora-OSRAM tubes at light intensity of 60 μmol/m2s) plus a red LED lamp SLP-838A-37 S1, λ max = 660 ± 20 nm, SANYO Electric Japan [7]. The red sample was subjected to a 16-hour photoperiod of which 12 hours with lighting provided by the OSRAM fluorescent Fluora tubes and the last 4 hours of the daily photoperiod with lighting only provided by the SLP-838A-37 S1, under the same climatic condition as above.

ACCEPTED MANUSCRIPT 2.2. Essential oil hydrodistillations After 4 months, the hydrodistillations were performed with a Clevenger-type apparatus equipped with an electric mantle heater. For each sample, 400 g FW were hydrodistilled for 5 hours. The yield is 0.05% for each hydrodistillation (0.05 g of EO, corresponding to 0.06 ml, for 100 g FW of parsley).

PT

2.3. Gas chromatography – Mass spectrometry Analyses

RI

The hydrodistilled essential oils were diluted to 5% in n-hexane HPLC grade and then injected into a GC-MS apparatus. Gas chromatography–electron impact mass spectrometry (GC–EI-MS) analyses

SC

were performed with a Varian CP-3800 gas chromatograph equipped with a DB-5 capillary column

NU

(30m×0.25 mm; coating thickness 0.25μm) and a Varian Saturn 2000 ion trap mass detector. Analytical conditions were: injector and transfer line temperatures 220 and 240 ◦C, respectively; oven

MA

temperature programmed from 60 to 240 ◦C at3 ◦C/min; carrier gas helium at 1 ml/min; injection of 0.2μl (5% n-hexane HPLC grade solution); split ratio 1:30. The identification of the constituents was

D

based on the comparison of the retention times with those of authentic samples, comparing their linear

PT E

retention indices relative to the series of n-hydrocarbons, on computer matching against commercial (NIST 14 and ADAMS) and laboratory-developed library mass spectra built up from pure substances

AC

in Figures 1-3.

CE

and components of known oils and MS literature data [8–12]. The obtained chromatograms are shown

PT E

D

MA

NU

SC

Figure 1. Chromatogram of the control sample essential oil.

RI

PT

ACCEPTED MANUSCRIPT

AC

CE

Figure 2. Chromatogram of the red-enriched sample essential oil.

Figure 3. Chromatogram of the red sample essential oil.

ACCEPTED MANUSCRIPT 2.4. Multivariate Statistical Analysis The multivariate statistical analyses were carried out with the JMP software package (SAS Institute, Cary, NC, USA). For the statistical evaluation of the volatile composition, the covariance data matrix was a 66 x 3 matrix (66 individual compounds x 3 samples = 198 data). The principal component analysis (PCA) was performed selecting the two highest principal components (PCs) obtained by the

PT

linear regressions operated on mean-centered, unscaled data; as an unsupervised method, this analysis

RI

aimed at reducing the dimensionality of the multivariate data of the matrix, whilst preserving most of

SC

the variance [13]. The chosen PC1 and PC2 cover 94.7 and 5.3% of the variance, respectively, for a total explained variance the complete dataset (100%). Both the HCA and the PCA methods can be

NU

applied to observe groups of samples even when there are no reference samples that can be used as a

MA

training set to establish the model. 3. Results and discussion

PT E

D

The complete compositions of the three EOs are reported in Table 1.

Table 1 Essential oil compositions of all the samples of Petroselinum crispum (Mill.) Fuss

CE

856 941 976 982 993 1001 1005 1027 1031 1042 1052 1062 1088 1089 1101 1102

Constituentsb

(E)-2-hexenal α-pinene sabinene β-pinene myrcene octanal α-phellandrene p-cymene β-phellandrene (Z)-β-ocimene (E)-β-ocimene γ-terpinene terpinolene p-cymenene linalool nonanal

AC

l.r.i.a

Relative abundance (%) CONTROL 0.2 0.8 0.3 4.7 1.2 0.2 17.2 0.1 0.3 7.1 2.5 -

RED-ENRICHED 0.3 1.1 0.1 0.5 3.7 2.0 0.2 26.0 0.2 0.3 5.3 1.8 -

RED -c 0.7 0.8 2.5 2.0 0.5 1.8 2.4 2.4 4.2 1.0 0.4 0.1

ACCEPTED MANUSCRIPT

CE

PT E

RI

PT

18.3 0.1 0.4 0.1 0.1 0.2 0.3 0.3 0.1 0.2 23.7 0.4 0.9 10.9 -

SC

NU

17.7 0.8 0.3 0.4 0.1 0.7 0.2 0.4 0.4 0.2 0.3 19.4 0.6 0.4 0.3 7.4 15.5 -

MA

D

1,3,8-p-menthatriene 1,5,8-p-menthatriene 4-terpineol p-methylacetophenone p-cymen-8-ol D-verbenone thymol methyl ether pulegone methyl carvacrol thymol carvacrol neo-isopulegol acetate α-copaene β-cubebene β-elemene β-caryophyllene β-copaene α-humulene (E)-β-farnesene γ-muurolene germacrene D bicyclogermacrene β-dihydro agarofuran α-muurolene α-bulnesene germacrene A (E,E)-α-farnesene β-bisabolene trans-γ-cadinene myristicin δ-cadinene trans-cadina-1(2),4-diene selina-3,7(11)-diene germacrene B dimethyl ionone (E)-nerolidol germacrene D-4-ol caryophyllene oxide carotol humulene epoxide II 1,10-di-epi-cubenol 1-epi-cubenol α-muurolol α-cadinol 7-epi-α-eudesmol β-bisabolol apiole caryophyllene acetate

AC

1113 1130 1178 1182 1183 1228 1235 1237 1241 1292 1298 1315 1376 1390 1392 1420 1429 1456 1460 1477 1481 1495 1498 1498 1505 1506 1507 1509 1513 1522 1524 1534 1542 1556 1563 1565 1575 1581 1594 1606 1614 1628 1645 1654 1655 1672 1684 1706

0.2 0.3 2.7 0.1 0.3 0.1 0.4 0.1 0.5 1.9 0.2 3.4 3.3 0.3 13.2 4.8 1.0 0.7 14.8 0.2 3.9 0.2 0.3 1.1 2.1 5.6 0.3 0.2 0.6 3.8 0.8 7.4 0.2 4.6

ACCEPTED MANUSCRIPT -

-

0.6 0.4

Total identified

99.5%

97.6%

99.2%

53.2 52.9 0.4 10.5 2.5 8.1 34.9 0.4 0.5

60.2 59.6 0.6 2.5 1.4 1.2 34.6 0.3

21.8 17.7 4.1 76.3 50.2 25.6 0.6 1.0

Monoterpenes, of which Hydrocarbons Oxygenated Sesquiterpenes, of which Hydrocarbons Oxygenated Sulphurated hydrocarbons Phenylpropanoids Apocarotenes Other on-terpene derivatives

PT

mint sulfide 2-ethylhexyl salicylate

RI

1739 1815

Linear retention indices calculated on a DB5 column; b Compounds listed according to elution order in a DB5 column; c Not detected.

NU

3.1. Control sample essential oil composition

SC

a

MA

The essential oil (EO) of the control sample was mainly rich in myristicin, a phenylpropanoid which represented the most abundant (19.4%) compound in this EO. Two monoterpene hydrocarbons, 1,3,8-

D

p-menthatriene and β-phellandrene, followed: they accounted for 17.7 and 17.2%, respectively.

PT E

Another relevant volatile organic compound (VOC) in this oil was apiole, another phenylpropanoid, whose relative abundance reached 15.5%. More than half (52.9%) of this EO was represented by

CE

monoterpene hydrocarbons, whilst phenylpropanoids accounted for 34.9%.

AC

3.2. Red-enriched sample essential oil composition The red-enriched sample essential oil was qualitatively similar to the control one, but with some differences in the relative abundances of the most relevant compounds. The most abundant VOC was β-phellandrene (26.0%), followed by the phenylpropanoid myristicin (23.7%); 1,3,8-p-menthatriene and apiole followed, accounting for 18.3 and 10.9%, respectively. Similarly to the control sample, the two most abundant chemical classes of VOCs were monoterpene hydrocarbons (59.6%) and phenylpropanoids (34.6%). The sesquiterpenes fraction was reduced: hydrocarbons accounted for 1.4%, whilst the oxygenated ones dropped to a 1.2% of relative abundance.

ACCEPTED MANUSCRIPT 3.3. Red sample essential oil composition The two most abundant compounds in this EO were (E,E)-α-farnesene (14.8%), a sesquiterpene hydrocarbon not detected in the other samples, and germacrene D (13.2%), whose relative abundance was less than 0.5% in the other EOs. Two oxygenated sesquiterpenes, not detected in the other EOs, follow: 7-epi-α-eudesmol and germacrene-D-4-ol accounted for 7.4 and 5.6%, respectively. The main

PT

differences in terms of composition for this EO were the absence of phenylpropanoids, which

RI

accounted for circa 35% in both the other samples, and the marked decrement of monoterpene

SC

hydrocarbons relative abundance to 17.7%. Sesquiterpenes represented the most abundant compounds in this sample EO: hydrocarbons constituted half of the composition (50.2%), while the

MA

they accounted for 4.1% in the red sample EO.

NU

oxygenated ones represented a quarter of it (25.6%). Oxygenated monoterpenes also increased, as

Among monoterpene hydrocarbons, α- and β-phellandrene showed a relevant decrement in their

D

relative abundances: the former was not detected in this EO, whilst the latter dropped to 2.4%.

PT E

Terpinolene and p-cymene, as well, disappeared from the EO composition, even though they were quite relevant in the other EOs. The opposite behavior was shown by (Z)- and (E)-β-ocimene, two other monoterpene hydrocarbons: the former accounted for 2.4% in this sample, whilst it was not

CE

present in the other EOs; the latter increased to 4.2%, whilst it accounted for 0.1 and 0.2% in the

AC

control and red-enriched samples, respectively. Among sesquiterpene hydrocarbons, other than (E,E)α-farnesene and germacrene D, also other compounds of this class, which showed a relevant presence in this EO, were not detected in the other samples: i.e. α-humulene (3.4%), bicyclogermacrene (4.8%) and δ-cadinene (3.9%). Other than 7-epi-α-eudesmol and germacrene-D-4-ol, two other oxygenated sesquiterpenes showed a significant relative abundance: (E)-nerolidol and caryophyllene acetate accounted for 2.1 and 4.6%, respectively, whilst they were not present in the other samples. 3.4. Multivariate statistical analysis

ACCEPTED MANUSCRIPT The hierarchical cluster analysis (HCA) dendrogram (Figure 4) of the total composition of the three

PT

essential oils showed a distribution of the samples in two groups.

RI

Figure 4 Hierarchical Cluster Analysis (HCA) dendrogram for the total composition of the analyzed essential oils

The red group comprises the control and the red-enriched samples, whose compositions are more

SC

similar compared to the red sample, which was clustered in the green cluster. The principal

NU

component analysis (PCA) further confirmed this distribution. Both the control and the red-enriched samples were in the left area (negative PC1) of the score plot (Figure 5), but the minor differences

AC

CE

PT E

D

MA

evidenced in their compositions are evident in the distance between these two samples.

Figure 5 Principal Component Analysis (PCA) score plot for the total composition of the analyzed essential oils

The former, indeed, was plotted in the upper quadrant (positive PC2), whilst the latter was positioned in the lower one (negative PC2). The RED sample was plotted in the lower right (positive PC1,

ACCEPTED MANUSCRIPT negative PC2) of the PCA plot, evidenced its more significant changes in the composition. The differences evidenced in the EOs composition, though, were statistically evidenced and confirmed. 4. Discussion The yields of extraction appeared uninfluenced by the used light treatment, accounting for 0.05%

PT

w/w for all the samples: also Petropoulos et al. (2008) and Borges et al. (2016) reported the same extraction yields for aerial parts of parsley specimens subjected to different stressful conditions, such

RI

as water deficiency.

SC

The composition of the control sample in the present study was similar to that reported in Ouis et al.

NU

(2014) for an EO hydrodistilled from a specimen of P. crispum from ex-Yugoslavia (the current name of the country is not reported), in which myristicin (60.5%), 1,3,8-p-menthatriene (20.1%) and β-

MA

phellandrene (6.2%) were the most abundant compounds. Also in Petropoulos et al. (2008), the EO of P. crispum subsp. crispum was mainly composed by myristicin (61.09%); β-phellandrene and

D

myrcene followed. Phenylpropanoids, specifically myristicin and apiole, were abundant compounds

PT E

in many P. crispum EOs from different countries: Serbia [16], Brazil [17] and Egypt [18]; other published EOs compositions showed the same behavior, but their geographical origin was not

CE

reported [19,20]. Monoterpene hydrocarbons were more abundant in the EOs hydrodistilled from Middle Eastern samples: Turkish parsley EO was mainly composed by 1,3,8-p-menthatriene, β-

AC

phellandrene, and myrcene [14]; 1,3,8-p-menthatriene, terpinolene, and myrcene were the most represented VOCs in the EO of Saudi Arabia parsley [14]; the Iranian sample in Ouis et al. (2014) showed an intermediate behavior between the last two EOs. Kiralan et al. (2012) reported an EO composition mainly composed by α- and β-pinene, followed by apiole and 2,3,4,5-tetramethoxy-1allylbenzene: the sample was from Mosul, Iraq. Comparing the red-enriched with the control sample, the major differences were the increment of almost 10% points of β-phellandrene and the decrement in the relative abundances of carotol (about 7%) and apiole (about 5%). Among the monoterpene hydrocarbons, myrcene, terpinolene, and p-

ACCEPTED MANUSCRIPT cymene showed a slight decrement, whilst 1,3,8-p-menthatriene was similar in terms of relative abundance. The phenylpropanoid myristicin showed an increment. The red sample EO showed much more relevant differences in its composition compared to both control and red-enriched samples. The main compounds of the control and red-enriched sample essential oils are phenylproanoids: they derive from trans-cinnamic acid, which is formed by phenylalanine amino acid in a reaction catalyzed

PT

by phenylalanine ammonium liase (PAL), whose activity in plants is highly regulated, as it is

RI

increased in response to biotic and abiotic stresses [22]. The activation of this enzyme, though,

SC

addresses the primary metabolism flux towards the phenylpropanoid pathway [23]. Indeed, an increment in the relative abundance myristicin was reported for parsley samples subjected to water

NU

stress: from an apiole-only composition in the control and moderate water stress level specimen EOs, the severe water stress treatment induced the presence of myristicin and β-sesquiphellandrene [24].

MA

This variation has been hypothesized as a defense mechanism of the plant, but the evidenced changes in the EO composition are different based on the cultivar, the growth conditions, etc. [25]. The

D

increment in myristicin was also reported in specimens of nutmeg (Myristica fragrans Houtt.)

PT E

subjected to dehydration stress: the higher content of this compound was found in the samples growing in the higher concentration of osmotic solution [26].

CE

In the control and red-enriched samples EOs of the present study, phenylpropanoids represented the

AC

second most abundant chemical class of compounds, whilst they were not detected in the red sample. This may lead to the hypothesis that the red light treatment is perceived as a less stressful environment for the parsley growth: the PAL enzyme, though, is not induced and the phenylpropanoids are not synthesized. Literature data on the phenylpropanoids pathway light-induced changes is quite scarce, and the precise biosynthetic reactions involved are not entirely clear. Phenols are a defense response against UV-induced damage [27]: the production of secondary metabolites of this chemical class is incremented by the treatment with supplementary UV-B irradiation even at early stages of parsley

ACCEPTED MANUSCRIPT specimens development [28]. In general, the parsley PAL enzyme is triggered by different kind of stressful events, but there are published works evidencing the opposite behavior. Microwaves (MW) irradiated parsley showed a decrement in its phenylpropanoids content (particularly myristicin), whilst the same treatment induced an increase of the phenylpropanoids in dill (Anethum graveolens L.) [29]. The MW radiation is a stress inductor in all the plants, thus the different reaction of parsley

PT

and dill to this stress could be explained as a difference in their defense mechanism, as the enzyme

RI

involved in the biosynthesis is the same.

SC

A second relevant change in the red sample EO composition is the increment of both the oxygenated mono- and sesquiterpenes. According to Nishioka et al. (2008), the photomorphogenic and

NU

photochemical responses to red wavelengths-enriched light treatments on Japanese mint plants induced a different effect of the light treatment on the different constituents of the essential oils: the

MA

results are reported for key-compounds only, anyway the red-enriched light seemed to increase the oxygenated compounds more than other wavelengths. The red light-induced increment in the

D

abundance of oxygenated compounds was also reported by Ivanitskikh and Tarakanov (2014): the

PT E

composition of the EOs hydrodistilled from Ocimum basilicum and Salvia officinalis both showed an increment in camphor and 1,8-cineole, compared with the other lighting growth conditions.

CE

Red light plays the most important role in the development of photosynthetic apparatus and influences

AC

morphogenesis by light-induced transformations of the phytochrome system [31]. Pisum sativum L. seedlings radiated with red light-emitting diode (LED) showed a relevant increment in the β-carotene expression [32]. Berries of Fragraria x ananassa (Duchesne ex Weston) Duchesne ex Rozier berries ripened over red wavelengths were about 20% larger, had higher sugar to organic acid ratios and emitted higher concentrations of favorable aroma compounds [33]. Light has potential to regulate the production of volatile molecules in plants, as well [34]. Red-light treatments, though, differently influenced the behavior of the same compounds in different species: this is due to the species-specific photochemical response to lighting conditions. Mulas et al. (2006)

ACCEPTED MANUSCRIPT studied the influence of red (660 nm) and far-red (730 nm) light on Rosmarinus officinalis EO composition: red photons caused an increment in α-pinene, like in the present study, whilst they decreased p-cymene relative abundance, which is the opposite of what was observed in this study. Halva et al. (1992) reported the composition of Anethum graveolens essential oil hydrodistilled from samples grown under different lighting conditions. As the EO of this study, p-cymene increased with

PT

the red-light treatment; they reported an increment in α-pinene, α- and β-phellandrene, whilst in the

RI

present study these compounds showed a decrease in their relative abundances [35].

SC

In the present work, the red-light enrichment of P. crispum growth induced slight differences for what concerns the essential oil composition: the chemotype and the most abundant chemical classes of

NU

volatile organic compounds were the same as the control sample. On the other hand, red lighting produced significant changes in the parsley essential oil composition, with a switch of chemotype and

MA

an increase in the relative abundance of oxygenated compounds. A scheme of the three samples behavior in terms of essential oils composition reactions to the different light environment is shown

AC

CE

PT E

D

in Figure 6.

ACCEPTED MANUSCRIPT Figure 6. Schematic of the compositional changes induced by the different light environments in the three analyzed samples. 5. Conclusions The effects induced by the three tested light treatments did not affect the essential oil extraction yields

PT

of the analyzed samples. Moreover, the red-enrichment was not sufficient to induce compositional changes. The red light only treatment, instead, caused significant differences in the essential oils

RI

chemical quality.

SC

The enrichment of the standard warm-white light in Petroselinum crispum growth, indeed, caused

NU

only some relative abundance changes in the essential oil composition: the chemotype was maintained and the main compounds were the same. The most abundant chemical classes of compounds were

MA

monoterpene hydrocarbons and phenylpropanoids: the two most relevant compounds in the composition of the red-light enriched sample essential oil were β-phellandrene and myristicin.

D

Major differences were detected in the essential oil hydrodistilled from the sample grown under red

PT E

light treatment, with a switch in the chemotype from myristicin, a phenylpropanoid, of the control sample to (E,E)-α-farnesene. The most abundant chemical classes of compounds were sesquiterpenes,

CE

both hydrocarbons and oxygenated ones: they were detected in low amounts in both the control and the red-enriched samples. Monoterpene hydrocarbons content dropped and phenylpropanoids were

AC

no longer present in this sample essential oil. These findings could lead to the hypothesis that the monochromatic red-light treatment is not perceived as a stressful environment by parsley, as in general the phenylpropanoids biosynthetic pathway is triggered by stressful events. Another possible explanation for this phenomena is the increased flux of the molecules involved in the phenylpropanoids biosynthesis towards non-volatile phenols in response to the different light radiation.

ACCEPTED MANUSCRIPT The light quality conditions are easy to modulate as needed: colored nets, fluorescent or LED lamps can be used to achieve different growth conditions. Further studies are needed to implement the change in the lighting treatment method to modulate the composition of the essential oil produced by plants grown under different light conditions. A wider number of species needs to be investigated as

PT

well, as the effect on the essential oil volatile compounds changes in different species. Conflict of interest

AC

CE

PT E

D

MA

NU

SC

RI

The authors have no conflict of interest to declare.

ACCEPTED MANUSCRIPT

References I.J. Warrington, K.J. Mitchell, The influence of blue- and red-biased light spectra on the growth and development of plants, Agric. Meteorol. 16 (1976) 247–262.

[2]

N. Nishioka, T. Nishimura, K. Ohyama, M. Sumino, S.H. Malayeri, E. Goto, N. Inagaki, T. Morota, Light Quality Affected Growth and Contents of Essential Oil Components of Japanese Mint Plants, Acta Hortic. 797 (2008) 431–436.

[3]

A. Noguchi, W. Amaki, Effects of light quality on the growth and essential oil production in Mexican mint, Acta Hortic. 1134 (2011) 239–244.

[4]

G. Mulas, Z. Gardner, L.E. Craker, Effect of Light Quality on Growth and Essential Oil Composition in Rosemary, Acta Hortic. 723 (2006) 427–431. doi:10.17660/ActaHortic.2016.1134.32.

[5]

D.S. Batista, K.M. de Castro, A.R. da Silva, M.L. Teixeira, T.A. Sales, L.I. Soares, M. das Graças Cardoso, M. de Oliveira Santos, L.F. Viccini, W.C. Otoni, Light quality affects in vitro growth and essential oil profile in Lippia alba (Verbenaceae), Vitr. Cell. Dev. Biol. Plant. 52 (2016) 276–282. doi:10.1007/s11627-016-9761-x.

[6]

S. Zhen, M.W. van Iersel, Far-red light is needed for efficient photochemistry and photosynthesis, J. Plant Physiol. 209 (2017) 115–122. doi:10.1016/j.jplph.2016.12.004.

[7]

K. Nishii, T. Nagata, C.N. Wang, M. Möller, Light as environmental regulator for germination and macrocotyledon development in Streptocarpus rexii (Gesneriaceae), South African J. Bot. 81 (2012) 50–60. doi:10.1016/j.sajb.2012.05.003.

[8]

E. Stenhagen, S. Abrahamsson, F.W. McLafferty, Registry of Mass spectral data, Wiley & Sons, New York, NY, 1974.

[9]

Y. Masada, Analysis of essential oils by gas chromatography and mass spectrometry, John Wiley & Sons, Inc., New York, NY, 1976.

[10]

W. Jennings, T. Shibamoto, Qualitative Analysis of Flavor and Fragrance Volatiles by Glass Capillary Gas Chromatography, Academic Press, New York, London, Sydney, Toronto, San Francisco, 1982.

[11]

N.W. Davies, Gas chromatographic retention indices of monoterpenes and sesquiterpenes on Methyl Silicon and Carbowax 20M phases, J. Chromatogr. A. 503 (1990) 1–24.

[12]

R.P. Adams, Identification of essential oil components by gas chromatography/quadrupole mass spectroscopy, Allured Publishing Corporation, Carol Stream, Illinois, USA, 1995.

[13]

Y.H. Choi, H.K. Kim, A. Hazekamp, C. Erkelens, A.W.M. Lefeber, R. Verpoorte, Metabolomic Differentiation of Cannabis sativa Cultivars Using 1H NMR Spectroscopy and Principal Component Analysis, J. Nat. Prod. 67 (2004) 953–957. doi:10.1021/np049919c.

[14]

N. Ouis, A. Hariri, A.D. El, Phytochemical analysis and antimicrobial bioactivity of the Algerian parsley essential oil (Petroselinum crispum), African J. Microbiol. Res. 8 (2014) 1157–1169. doi:10.5897/AJMR12.1021.

[15]

S.A. Petropoulos, D. Daferera, M.G. Polissiou, H.C. Passam, The effect of water deficit stress on the growth, yield and composition of essential oils of parsley, Sci. Hortic.

AC

CE

PT E

D

MA

NU

SC

RI

PT

[1]

ACCEPTED MANUSCRIPT (Amsterdam). 115 (2008) 393–397. doi:10.1016/j.scienta.2007.10.008. M. Stankovic, N. Nikolic, L. Stanojevic, M. Cakic, The effect of hydrodistillation technique on the yield and composition of essential oil from the seed of petroselinum crispum (mill.) Nym. Ex. A.W. Hill, Hem. Ind. 58 (2004) 409–412. doi:10.2298/HEMIND0409409S.

[17]

J. Camilotti, L. Ferarrese, W. De Campos Bortolucci, J.E. Gonçalves, O.S. Takemura, R.J. Piau, O. Alberton, G.A. Linde, Z.C. Gazim, Essential oil of parsley and fractions to in vitro control of cattle ticks and dengue mosquitoes, J. Med. Plants Res. 9 (2015) 1021–1030. doi:10.5897/JMPR2015.5941.

[18]

R.M. Romeilah, S.A. Fayed, G.I. Mahmoud, Chemical Compositions, Antiviral and Antioxidant Activities of Seven Essential Oils, J. Appl. Sci. Res. 6 (2010) 50–62.

[19]

H. Zhang, F. Chen, X. Wang, H.-Y. Yao, Evaluation of antioxidant activity of parsley (Petroselinum crispum) essential oil and identification of its antioxidant constituents, Food Res. Int. 39 (2006) 833–839. doi:10.1016/j.foodres.2006.03.007.

[20]

G.A. Linde, Z.C. Gazim, B.K. Cardoso, L.F. Jorge, V. Tešević, J. Glamoćlija, M. Soković, N.B. Colauto, Antifungal and antibacterial activities of Petroselinum crispum essential oil, Genet. Mol. Res. 15 (2016). doi:10.4238/gmr.15038538.

[21]

M. Kiralan, A. Bayrak, O.F. Abdulaziz, T. Özbucak, Essential oil composition and antiradical activity of the oil of Iraq plants, Nat. Prod. Res. 26 (2012) 132–139. doi:10.1080/14786419.2010.535149.

[22]

R.A. Dixon, N.L. Paiva, Stress-Induced Phenylpropanoid Metabolism., Plant Cell. 7 (1995) 1085–1097. doi:10.1105/tpc.7.7.1085.

[23]

C. LILLO, U.S. LEA, P. RUOFF, Nutrient depletion as a key factor for manipulating gene expression and product formation in different branches of the flavonoid pathway, Plant. Cell Environ. 31 (2008) 587–601. doi:10.1111/j.1365-3040.2007.01748.x.

[24]

B.B. Ivania, K.C. Bruna, S.S. Elo iacute sa, S. de O. J eacute ssica, F. da S. Rafael, M. de R. Cl aacute udia, E.G. ccedil alves Jos eacute, P.J. Ranulfo, G.H. de S. Silvia, C.G. Zilda, Evaluation of performance and chemical composition of Petroselinum crispum essential oil under different conditions of water deficit, African J. Agric. Res. 11 (2016) 480–486. doi:10.5897/AJAR2015.10748.

[25]

L. Aparecida, S. De Morais, R.F. Castanha, Composição química do óleo essencial de manjericão naturalmente submetido ao ataque de cochonilhas ., Hortic. Bras. 30 (2012) 2178–2182. https://www.alice.cnptia.embrapa.br/alice/bitstream/doc/951008/1/2012AA56.pdf (accessed February 14, 2018).

[26]

N. Rahman, T.B. Xin, H. Kamilah, F. Ariffin, Effects of osmotic dehydration treatment on volatile compound (Myristicin) content and antioxidants property of nutmeg (Myristica fragrans) pericarp, J. Food Sci. Technol. 55 (2018) 183–189. doi:10.1007/s13197-017-28832.

[27]

K. Hahlbrock, D. Scheel, Physiology and Molecular Biology of Phenylpropanoid Metabolism, Annu. Rev. Plant Physiol. Plant Mol. Biol. 40 (1989) 347–369. doi:10.1146/annurev.pp.40.060189.002023.

[28]

C.B. Johnson, J. Kirby, G. Naxakis, S. Pearson, Substantial UV-B-mediated induction of essential oils in sweet basil (Ocimum basilicum L.), Phytochemistry. 51 (1999) 507–510. doi:10.1016/S0031-9422(98)00767-5.

AC

CE

PT E

D

MA

NU

SC

RI

PT

[16]

ACCEPTED MANUSCRIPT I. Lung, M. Stan, O. Opriş, M.-L. Soran, Determination of Myristicin and Linalool in Plants Exposed to Microwave Radiation by High-Performance Liquid Chromatography, Anal. Lett. 48 (2015) 567–574. doi:10.1080/00032719.2014.954120.

[30]

A.S. Ivanitskikh, I.G. Tarakanov, Effect of Light Spectral Quality on Essential Oil Components in Ocimum Basilicum and Salvia Officinalis Plants, Int. J. Second. Metab. 1 (2014) 19.

[31]

A. Urbonavičiute, P. Pinho, G. Samuoliene, P. Duchovskis, P. Vitta, G. Stonkus, A. Tamulaitis, A. Zukauskas, L. Halonen, Effect of Short-Wavelength Light on Lettuce Growth and Nutritional Quality, Sci. Work. Lith. Inst. Hortic. Lith. Univ. Agric. - Sodininkystė Ir Daržininkystė. 26 (2007) 157–165.

[32]

M.-C. Wu, C.-Y. Hou, C.-M. Jiang, Y.-T. Wang, C.-Y. Wang, H.-H. Chen, H.-M. Chang, A novel approach of LED light radiation improves the antioxidant activity of pea seedlings, Food Chem. 101 (2007) 1753–1758. doi:10.1016/J.FOODCHEM.2006.02.010.

[33]

M.J. Kasperbauer, J.H. Loughrin, S.Y. Wang, Light Reflected from Red Mulch to Ripening Strawberries Affects Aroma, Sugar and Organic Acid Concentrations, Photochem. Photobiol. 74 (2007) 103–107. doi:10.1562/0031-8655(2001)0740103LRFRMT2.0.CO2.

[34]

X. Fu, Y. Chen, X. Mei, T. Katsuno, E. Kobayashi, F. Dong, N. Watanabe, Z. Yang, Regulation of formation of volatile compounds of tea (Camellia sinensis) leaves by single light wavelength, Sci. Rep. 5 (2015) 16858. doi:10.1038/srep16858.

[35]

S. Halva, L.E. Craker, J.E. Simon, D.J. Charles, Light quality, growth and essential oil in dill (Anethum graveolens L.), J. Herbs, Spices Med. Plants. 1 (1992) 59–70. doi:10.1300/J044v01n01_07.

AC

CE

PT E

D

MA

NU

SC

RI

PT

[29]

ACCEPTED MANUSCRIPT Highlights

CE

PT E

D

MA

NU

SC

RI

PT

The effect of different lighting conditions on parsley essential oil was evaluated The red-light enrichment caused slight changes in the essential oil composition The red lighting caused major changes in the EO, including the chemotype switch Different lighting conditions could modulate the essential oil composition

AC

1. 2. 3. 4.