Plutella xylostella (L.) infestations at varying temperatures induce the emission of specific volatile blends by Arabidopsis thaliana (L.) Heynh

Dieu-Hien Truong; Benjamin M Delory; Yves Brostaux; Stéphanie Heuskin; Pierre Delaplace; Frédéric Francis; Georges Lognay

doi:10.4161/15592324.2014.973816

. 2014 Oct 31;9(11):e973816. doi: 10.4161/15592324.2014.973816

Plutella xylostella (L.) infestations at varying temperatures induce the emission of specific volatile blends by Arabidopsis thaliana (L.) Heynh

Dieu-Hien Truong ^1,^2,^3,^*, Benjamin M Delory ⁴, Yves Brostaux ⁵, Stéphanie Heuskin ¹, Pierre Delaplace ⁴, Frédéric Francis ², Georges Lognay ^1,^*

PMCID: PMC4622421 PMID: 25482777

Abstract

The effect of combined abiotic and biotic factors on plant volatile organic compound (VOC) emissions is poorly understood. This study evaluated the VOC emissions produced by Arabidopsis thaliana (L.) Col-0 subjected to 3 temperature regimes (17, 22, and 27°C) in the presence and absence of Plutella xylostella larvae over 2 time intervals (0–4 and 4–8 h), in comparison to control plants. The analyses of VOCs emitted by Arabidopsis plants were made by headspace solid phase microextraction (HS-SPME) coupled with gas chromatography-mass spectrometry (GC-MS). It was found that certain volatile groups (e.g., alcohols, ketones, aldehydes, and terpenes) are induced by both single factors (temperature or larval infestation) and combined factors (temperature and larvae interactions), whereas other volatile groups (e.g., isothiocyanates [ITCs] and nitrile) were specific to the experimental conditions. ITCs (mainly 4-methylpentyl isothiocyanate) were emitted from plants subjected to larval infestation at 17 and 27°C after the 2 time intervals. The proportions of sulfides (mainly dimethyl disulfide) and 4-(methylthio) butanenitrile were significantly higher on herbivore-infested plants at 22°C compared to the other treatments. Overall, our findings indicate that changes in all experimental conditions caused significant changes to the VOC emissions of Arabidopsis plants. Therefore, the interaction between temperature and larval feeding may represent an important factor determining the variability of volatile emissions by plants subjected to multiple simultaneous factors.

Keywords: Arabidopsis thaliana, combined factors, Plutella xylostella, temperature regimes, volatile organic compounds (VOCs)

Introduction

Under natural growing conditions, plants are often challenged by many environmental stresses that may occur simultaneously. Such stresses influence the primary and secondary metabolisms of higher plants.^1-5 Many volatile organic compounds (VOCs) are synthesized, stored in specific plant parts (e.g., glandular trichomes, oil, and resin ducts) and released in response to abiotic and/or biotic factors.^2,6 The main pathways leading to VOC biosynthesis include the mevalonate (MVA) pathway (in the cytosol/endoplasmic reticulum; producing sesquiterpenoids) and the 2-C-methyl-D-erythritol 4-phosphate (MEP) pathway (in plastids; liberating mono- and diterpenoids), the shikimic acid pathway (for phenylpropanoid and benzenoid compounds), and the lipoxygenase/hydroperoxide lyase (LOX/HPL) pathway (for green leaf volatiles [GLVs]), along with the myrosinase-catalyzed degradation of glucosinolates (GSs).^1,7-11 Evidence shows that the abiotic stress factors may change the photochemical or biochemical processes of the photosynthetic cycle.² Therefore, VOC emissions might be influenced by changes in biosynthetic pathways (e.g., terpenoids and GLVs).^2,12 Existing data also indicate that plants respond to biotic stresses by emitting specific blends of volatiles through plant defensive responses regulated by a signaling network, in which salicylate (SA), jasmonate (JA), and ethylene (ET) play key roles.^8,13-17

Among the various abiotic factors, temperature is a major environmental stressor that directly affects plant inflorescence development, physiological processes and also influences the evaporation and release of VOCs.^2,18 It has been suggested that the release of plant VOCs is frequently associated to an increase or decrease in temperature.^1,219,20 For example, Gouinguené and Turlings¹⁹ found that higher VOC emissions were obtained from corn plants (Zea mays L.) subjected to temperatures between 22 and 27°C compared to lower and higher temperatures. Changes in VOC emissions at different temperatures are often linked to the vapor pressure changes and stomatal behavior of plants. For instance, rising temperature leads to an increase in the rate of volatile production (e.g., isoprene, monoterpenes, and sesquiterpenes).¹ The temperature-dependent opening and closing of stomata might affect the rate of VOC emission. For example, stomatal closure reduces oxygenated VOCs (e.g., methanol, C6 aldehydes, and other alcohols).^2,21

Feeding and oviposition by herbivorous insects are well-documented biotic factors that influence the emission of plant volatiles.^1,22-25 Holopainen and Gershenzon¹ reported that the emission of terpenes and GLVs may be induced by herbivorous attack. Studies on plant-herbivore interactions have proposed that the release of VOCs is strongly correlated to the type of insect pest and experimental conditions.^13,26-29 Ali and Agrawal³⁰ recorded that phloem-sap feeders (Rhopalosiphum maidis) do not increase volatile emissions in Z. mays, whereas chewers (Spodoptera littoralis) strongly induce the production of many VOCs.

Existing data show that chewing insects cause extensive damage to plant cells following infestation, with mechanical damage and oral secretions acting as major signals that trigger the release of volatiles from plants.^30-33 Studies on the direct (repellent, feeding deterrents, or toxins) or indirect (attractants and/or feeding or oviposition stimulants for organisms of the third trophic level) defenses of Arabidopsis against caterpillars have shown that VOC emissions may be induced through the JA signaling pathway by lepidopteran attacks.^8,30,34 The diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae), is a chewing insect that specializes on the Brassicaceae plants, and causes many Brassica species to emit volatiles.^35-37 For example, Vuorinen et al.³⁷ found that some terpenes (e.g., (E)-4,8-dimethyl-1,3,7-nonatriene and (E,E)-α-farnesene) and one GLV ((Z)-3-hexenyl acetate) are released by P. xylostella-infested cabbage plants. Van Poecke⁸ reported that the level of aliphatic GS is positively correlated with the damage caused by P. xylostella. Although the diamondback moth accepts Arabidopsis thaliana as a host plant,³⁸ the change in volatile profiles that are emitted following infestation has received limited focus.³⁹

Plants are often subjected to multiple simultaneously occurring factors under natural conditions, resulting in altered VOC emission patterns. However, much less is known about the emission of VOC blends during plant responses to such multiple factors.^1,40,41 In this study, the co-occurrence of abiotic (different temperatures) and biotic (P. xylostella larval feeding pressure) factors were applied to A. thaliana Col-0 plants under controlled conditions. This work aimed at evaluating how a combination of different temperature regimes and feeding by P. xylostella larvae affected Arabidopsis VOC emissions over different time intervals. We investigated whether Arabidopsis plants exposed to a single factor treatment versus combined factor treatments exhibited different volatile profiles. These results are expected to determine the components of VOC reaction products in plant–multiple factor interactions.

Results

The identified volatile compounds emitted by A. thaliana in our experimental conditions are presented in Table 1. Overall, 19 volatile compounds belonging to 8 VOC classes (terpenes, sulfides, nitrile, ketones, alcohols, aldehydes, isothiocyanates [ITCs], and ester) were detected among the various conditional treatments (Table 1). Principal component analyses (PCAs) confirmed variations in the volatile profiles emitted by Arabidopsis plants making it possible to discriminate between uninfested and infested plants at different temperatures over the 2 time intervals. First, PCA using the relative abundances of each individual compound captured 45.4% of the total variance on score plot constructed with the 2 first principal components (PCs) (i.e., PC1 26.9% and PC2 18.5%; Fig. 1A). Statistical correlations between variables and PCs (based on PC1 and PC2 score plots) indicated that PC1 was positively correlated with 6-methyl hept-5-en-2-one (0.41), (E,E)-α-farnesene (0.36), 2-ethylhexan-1-ol (0.34), octan-2-one (0.34), nonan-2-one (0.25), and heptan-2-one (0.18). Geranyl acetone (PC1: −0.03; PC2: 0.23), dimethyl disulfide (DMDS; PC1: −0.23; PC2: 0.21), 4-(methylthio) butanenitrile (PC1: −0.35; PC2: 0.23), benzaldehyde (PC1: −0.37; PC2: 0.12), limonene (PC1: −0.57; PC2: 0.50), cyclohexanone (PC1: −0.69; PC2: 0.26), and menthol (PC1: −0.81; PC2: 0.39) were negatively correlated with PC1 and positively correlated with PC2. In contrast, both PC1 and PC2 were positively correlated with 4-methylpentyl ITC (PC1: 0.77; PC2: 0.52), pent-1-en-3-ol (PC1: 0.75; PC2: 0.45), methyl salicylate (MeSA; PC1: 0.72; PC2: 0.49), heptyl ITC (PC1: 0.69; PC2: 0.36), 2-ethylhexanal (PC1: 0.58; PC2: 0.10), and dimethyl trisulfide (DMTS; PC1: 0.49; PC2: 0.64). In addition, PCA using the relative abundance of each VOC class accounted for 62.3% of the total observed variation on score plots constructed with PC1 (38.5%) and PC2 (23.8%) (Fig. 1B). The analysis of score plots constructed with PC1 and PC2 indicated that PC1 was positively correlated with alcohols (0.73) and ketones (0.49), but was negatively correlated with sulfides (−0.70) and nitrile (−0.75). In contrast, PC2 was negatively correlated with alcohols (−0.22) and ketones (−0.55), but positively correlated with sulfides (0.49) and nitrile (0.30). Both PC1 and PC2 were positively correlated with aldehydes (PC1: 0.56; PC2: 0.24), ITCs (PC1: 0.54; PC2: 0.75), and ester (PC1: 0.53; PC2: 0.77), but negatively correlated with terpenes (PC1: −0.61; PC2: −0.08).

Table 1.

Mean relative abundances (n = 3; ± SD) of VOCs emitted by A. thaliana subjected to different temperature regimes (17, 22, and 27°C) or to temperature regimes combined with P. xylostella larval infestation (9 larvae per plant) over 2 time intervals (0–4 and 4–8 h)

				Uninfested						Infested by 9 Plutella xylostella larvae per plant
				VOC proportion (%)^(IV)
				0–4 h			4–8 h			0–4 h			4–8 h
Compound	RIcal^(I)	RIref^(II)	Identification^(III)	17°C	22°C	27°C	17°C	22°C	27°C	17°C	22°C	27°C	17°C	22°C	27°C
Terpenes
Limonene	1026	1029	MS, KI⁷⁴	3.21 ± 2.18^ab	4.64 ± 0.55^ab	0.25 ± 0.23^b	4.98 ± 2.31^ab	8.16 ± 2.71^a	0.15 ± 0.11^b	2.74 ± 1.02^ab	3.22 ± 2.72^ab	0.39 ± 0.29^b	1.97 ± 0.58^b	3.96 ± 3.85^ab	1.06 ± 0.39^b
Menthol	1172	1171	MS, KI⁷⁵	7.51 ± 2.74^d	43.56 ± 1.35^a	6.92 ± 1.52^d	5.85 ± 0.56^d	47.62 ± 0.86^a	4.46 ± 0.50^d	7.57 ± 1.25^d	28.61 ± 1.94^b	7.47 ± 1.49^d	7.75 ± 2.45^d	17.73 ± 3.^14c	6.52 ± 1.42^d
(E,E)-α-farnesene	1537	1506	MS, KI⁵⁵	nd	nd	nd	nd	nd	nd	nd	nd	trace	nd	nd	2.03 ± 0.76^a
Total terpenes				10.74 ± 0.92^d	48.20 ± 1.68^ab	7.17 ± 1.41^d	10.83 ± 2.55^d	55.78 ± 3.57^a	4.61 ± 0.60^e	10.31 ± 1.60^d	31.84 ± 4.27^bc	7.86 ± 1.56^d	9.72 ± 2.06^d	21.69 ± 1.27^c	9.61 ± 1.01^d
Sulfides
Dimethyl disulfide	646	-	MS ²²	nd	nd	nd	nd	nd	nd	3.46 ± 0.75^c	7.74 ± 1.26^b	trace	2.32 ± 0.69^d	54.71 ± 5.52^a	5.85 ± 0.65^b
Dimethyl trisulfide	964	964	MS, KI⁵⁵	nd	nd	nd	nd	nd	nd	4.41 ± 1.34^a	2.77 ± 1.47^abc	1.24 ± 0.21^c	2.99 ± 0.54^ab	2.22 ± 0.61^abc	1.54 ± 0.54^bc
Total sulfides										7.87 ± 0.63^c	10.51 ± 0.25^b	1.24 ± 0.21^e	5.31 ± 1.19^d	56.93 ± 5.34^a	7.39 ± 0.39^c
Nitrile
4-(methylthio) butanenitrile	1116	-	MS ⁷⁶	nd	nd	nd	nd	nd	nd	nd	3.99 ± 0.16^a	nd	trace	3.31 ± 0.39^b	trace
Ketones
Heptan-2-one	897	892	MS, STD, KI⁷⁴	nd	nd	14.21 ± 8.52^a	nd	nd	23.80 ± 9.42^a	nd	trace	3.75 ± 1.43^b	1.46 ± 0.59^c	3.04 ± 1.79^b	11.33 ± 3.23^a
Cyclohexanone	917	895	MS, STD, KI⁷⁷	nd	1.35 ± 0.08^b	nd	nd	2.28 ± 0.58^a	nd	nd	nd	nd	nd	nd	nd
6-Methyl hept-5-en-2-one	986	986	MS, STD, KI⁵⁵	15.79 ± 6.17^a	1.45 ± 0.33^c	10.90 ± 4.98^ab	7.17 ± 1.45^bc	1.10 ± 0.25^c	4.70 ± 1.78^bc	8.20 ± 2.37^bc	3.52 ± 0.50^bc	8.41 ± 0.36^abc	5.47 ± 1.16^bc	1.13 ± 0.27^c	2.37 ± 0.96^c
Octan-2-one	991	991	MS, STD, KI⁷⁴	nd	nd	1.58 ± 0.86^a	nd	nd	1.71 ± 0.62^a	nd	nd	1.79 ± 1.49^a	nd	nd	2..22 ± 1.35^a
Nonan-2-one	1108	1090	MS, STD, KI⁷⁴	1.13 ± 0.35^f	nd	7.74 ± 0.96^c	5.57 ± 0.66^cd	nd	34.63 ± 3.85^a	trace	2.81 ± 0.22^e	4.66 ± 1.19^d	7.78 ± 0.89^c	1.39 ± 0.59^f	14.32 ± 1.26^b
Geranyl acetone	1154	1154	MS, STD, KI²⁸	15.95 ± 6.25^abc	17.61 ± 2.24^ab	12.35 ± 6.10^bcd	23.95 ± 7.32^a	10.23 ± 1.96^bcd	5.54 ± 1.99^cd	17.70 ± 3.55^ab	7.14 ± 1.99^bcd	6.82 ± 1.16^bcd	8.96 ± 1.93^bcd	2.85 ± 1.19^d	3.20 ± 1.22^d
Total ketones				32.87 ± 2.65^cde	20.41 ± 1.98^fg	46.78 ± 1.88^b	36.69 ± 6.44^c	13.61 ± 2.70^gh	70.39 ± 2.92^a	25.90 ± 3.77^def	13.47 ± 2.32^gh	25.41 ± 1.98^def	23.67 ± 3.91^ef	8.42 ± 2.25^h	33.45 ± 1.74^cd
Alcohols
Pent-1-en-3-ol	607	673	MS, STD, KI⁵⁵	nd	nd	nd	nd	nd	nd	3.74 ± 2.56^a	trace	1.21 ± 0.61^b	4.22 ± 1.80^a	trace	2.76 ± 0.97^ab
2-Ethylhexan-1-ol	1029	1033	MS, STD, KI⁵⁵	39.71 ± 2.71^ab	23.25 ± 1.69^cd	32.12 ± 5.18^bc	43.80 ± 3.72^ab	22.52 ± 4.35^cd	19.05 ± 2.54^d	25.85 ± 5.69^cd	26.55 ± 3.81^cd	50.64 ± 6.26^a	28.83 ± 4.11^bcd	4.44 ± 0.39^e	28.29 ± 2.07^bcd
Total alcohols				39.71 ± 2.71^bc	23.25 ± 1.69^de	32.12 ± 5.18^cd	43.80 ± 3.72^ab	22.52 ± 4.35^de	19.05 ± 2.54^e	29.59 ± 5.69^cde	26.55 ± 3.81^de	51.84 ± 5.86^a	33.05 ± 3.49^bcd	4.44 ± 0.39^f	31.06 ± 1.19^cd
Aldehydes
2-Ethylhexanal	952	954	MS, STD, KI⁷⁸	16.68 ± 2.32^a	1.57 ± 0.64^f	10.20 ± 1.59^bc	8.68 ± 0.50^bc	1.44 ± 0.69^f	2.54 ± 0.88^ef	10.21 ± 0.66^bc	8.84 ± 2.41^bc	6.35 ± 1.04^cde	11.13 ± 1.04^b	2.85 ± 1.58^def	6.50 ± 0.73^cd
Benzaldehyde	958	960	MS, STD, KI⁷⁹	nd	6.57 ± 1.51^a	3.73 ± 2.25^a	nd	6.65 ± 1.16^a	3.41 ± 0.32^a	3.26 ± 0.81^a	4.81 ± 2.95^a	4.92 ± 2.25^a	3.21 ± 0.74^a	2.36 ± 1.39^a	3.53 ± 1.06^a
Total aldehydes				16.68 ± 2.32^a	8.14 ± 2.13^de	13.93 ± 2.91^ab	8.68 ± 0.50^cde	8.09 ± 0.48^de	5.95 ± 0.57^e	13.47 ± 0.90^abc	13.65 ± 0.83^abc	11.27 ± 2.30^bcd	14.34 ± 1.69^ab	5.21 ± 2.39^e	10.02 ± 1.33^bcde
Isothiocyanates (ITCs)
4-Methylpentyl ITC	1177	1148	MS, KI⁵⁵	nd	nd	nd	nd	nd	nd	5.12 ± 1.26^a	nd	0.61 ± 0.37^c	5.01 ± 0.43^a	nd	3.28 ± 0.17^b
Heptyl ITC	1281	1253	MS, KI⁵⁵	nd	nd	nd		nd	nd	2.95 ± 0.57^a	nd	1.21 ± 0.58^bc	0.77 ± 0.15^c	nd	1.83 ± 0.88^ab
Total ITCs										8.07 ± 1.78^a		1.82 ± 0.62^c	5.78 ± 0.47^ab		5.11 ± 1.05^b
Ester
Methyl salicylate	1193	1192	MS, STD, KI⁵⁵	nd	nd	nd	nd	nd	nd	4.79 ± 0.23^b	trace	0.54 ± 0.10^d	8.14 ± 0.46^a	trace	3.36 ± 0.61^c

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nd = not detected; trace (< 0.05%); *: over estimated value

^(I)

Linear Retention index calculated for Restek Rtx-502.2 column (5%phenyl/95%methylpolysiloxane, USA) (32 m × 0.25 μm × 0.25 mm i.d.) with a homologous series of n-alkanes (C7–C30).

^(II)

Linear Retention index in literature.

^(III)

Identification proposal is indicated as followings: MS, identification by comparing EI mass spectrum with the Wiley and NIST MS 2.0 mass spectral databases; RI, identification by Retention indexes with the literature data; STD, comparison with the retention times and mass spectra of available authentic compounds.

^(IV)

For each individual VOC or each chemical family, mean values sharing the same letter in the same row do not statistically differ (P > 0.05, 3-way ANOVA, post hoc Tukey's HSD test).

Figure 1. — Principal component analyses (PCAs) and hierarchical clustering analysis (HCA) of VOC profiles emitted by *A. thaliana* subjected to different temperature regimes (17, 22, and 27°C) or to temperature regimes combined with *P. xylostella* larval infestation (9 larvae per plant) over 2 time intervals (0–4 and 4–8 h). PCAs show the first (PC1) and second (PC2) principal components. Uninf: uninfested plants; Inf: infested plants. (A) PCA based on individual VOC relative abundances. (B) PCA and (C) HCA based on the relative proportions of each chemical family in VOC blends emitted by *A. thaliana*.

The hierarchical clustering analysis (HCA) performed on PCs separated the chemical profiles emitted by plants infested and uninfested by P. xylostella larvae at different temperatures into 3 clusters (Fig. 1C). The first cluster (Group 1 in the PCA) primarily consisted of volatile blends emitted from uninfested and infested Arabidopsis plants maintained at 22°C. Volatile profiles released by uninfested plants analyzed at 17 and 27°C corresponded to the second cluster (Group 2 in PCA). Chemical profiles emitted by infested Arabidopsis plants at the highest temperature (27°C) after 0–4 h were also included in this group. Finally, the third cluster (Group 3 in PCA) contained volatile blends emitted by infested Arabidopsis plants analyzed at 17°C, in addition to volatile profiles released by infested plants at 27°C after 4–8 h (Fig. 1B and C). The coefficients of correlation between PCs and variables indicated that the chemical profiles emitted from Arabidopsis plants in Cluster 1 were characterized by sulfides, nitrile, and terpenes, Cluster 2 by alcohols and ketones, and Cluster 3 by aldehydes, ITCs, and ester.

To identify differences in the emission of volatile profiles between experimental treatments corresponding to the 3 clusters already distinguished by HCA, 3-way ANOVA was carried out for each VOC class, as well as their specific compounds, followed by a post hoc Tukey's test. The results showed that terpenes had the highest proportions on uninfested Arabidopsis plants at 22°C in comparison with the other experimental treatments (P < 0.001; Cluster 1; Fig. 2A). The chemical profiles produced by infested plants at 17 and 22°C were characterized by a decrease in terpene proportions compared to uninfested plants for both time intervals. When considering the specific compounds, (E,E)-α-farnesene was only detected from infested plants at 27°C after the second time interval. The highest proportions of menthol were obtained from uninfested Arabidopsis plants at 22°C over the 2 time periods (P < 0.001). In contrast, there was no significant interaction between temperature and larval infestation over the 2 time intervals on the proportion of limonene among experimental conditions (p = 0.443; Table 1).

Figure 2. — Mean relative abundance (% ± SD; n = 3) of each VOC chemical family emitted by *A. thaliana* subjected to different temperature regimes (17, 22, and 27°C) or to temperature regimes combined with *P. xylostella* larval infestation (9 larvae per plant) over 2 time intervals (0–4 and 4–8 h). Uninf: uninfested plants; Inf: infested plants. Means sharing the same letter are not statistically different (P > 0.05, 3-way ANOVA, *post hoc* Tukey's HSD test).

In contrast to terpenes, sulfides (P < 0.001) and nitrile (p = 0.004) had the highest proportions when Arabidopsis plants were infested by P. xylostella and analyzed at 22°C (Cluster 1; Fig. 2B and C). When considering the single sulfides, DMDS (P < 0.001) and DMTS (p = 0.385) levels increased in plants subjected to larval infestation at 22°C in comparison with the other conditional treatments. Similarly, the release of 4-(methylthio) butanenitrile (the only detected nitrile; p = 0.004) generally occurred on infested plants at 22°C (Table 1).

With respect to ketones, the relative abundances were higher when plants were exposed to temperature treatments at 27°C after the second time interval in comparison with the other experimental treatments (p = 0.009; Cluster 2; Fig. 2D). With respect to the single compounds, the proportions of cyclohexanone (p = 0.002), nonan-2-one (P < 0.001), and geranyl acetone (p = 0.004) significantly varied in plants exposed to different treatments. However, there was no significant interaction between temperature and larval infestation over the 2 time periods on the proportions of heptan-2-one (p = 0.223), 6-methyl hept-5-en-2-one (p = 0.160), and octan-2-one (p = 0.940) (Table 1).

Like ketones, the highest proportion of total alcohols was obtained in the volatile blends released by Arabidopsis plants subjected to larval infestation at 27°C after the first time interval (p = 0.009; Cluster 2; Fig. 2E). With respect to individual compounds, pent-1-en-3-ol was only detected from plants exposed to combined temperature and larval treatments (p = 0.273). In comparison, the relative abundance of 2-ethylhexan-1-ol decreased at 17 and 22°C, but increased at 27°C, on infested Arabidopsis plants compared to uninfested samples (p = 0.014) (Table 1).

The proportion of aldehydes (P < 0.001) was significantly higher on uninfested Arabidopsis plants at 17 and 27°C after 0–4 h (Cluster 2, Fig. 2F). In contrast, the highest proportions of ITCs (P < 0.001), and MeSA (the only detected ester; P < 0.001) were generally obtained for plants subjected to larval infestation at 17 and 27°C in comparison with the other treatments over the 2 time intervals (Cluster 3; Fig. 2G and H). With respect to individual compounds, the relative abundance of 2-ethylhexanal significantly increased on infested plants compared to uninfested samples after the second time interval (P < 0.001), whereas no significant variation was observed for benzaldehyde among experimental treatments (p = 0.580). The emission of ITCs, 4-methylpentyl ITC (P < 0.001), and heptyl ITC (P < 0.001) were only detected from plants subjected to larval infestation at 17 and 27°C after 0–4 and 4–8 h treatments (Table 1).

Discussion

Biotic (herbivorous insects, fungi, pathogens) and abiotic (temperature, drought, salt) plant factors commonly occur simultaneously in the natural environment.^1,40 Previous studies have demonstrated that the combination of abiotic stresses (water, drought and heavy metal) and herbivory causes the weakening or strengthening of plant VOC emissions in comparison with single stress treatments.^3,41 Recently, our research group reported that the combined temperature-herbivory (aphid, M. persicae) interaction causes the volatile profile of Arabidopsis plants to change.⁴² In the current study, we observed strong changes in the relative proportions of both individual compounds and VOC chemical families comprising the volatile blends released by 5-week-old A. thaliana plants infested or not by P. xylostella and analyzed at varying temperatures (Fig. 1 and 2, and Table 1). We found that volatile profiles from infested Arabidopsis at different temperatures were characterized by the emission of ester, ITCs, aldehydes, sulfides, and nitrile. In contrast, the VOC profiles of uninfested plants were characterized by alcohols, ketones, aldehydes, and terpenes (Fig. 2).

This study confirmed that simultaneous abiotic and biotic factors affect plant volatile emission. The combination of temperature regimes and P. xylostella larval infestation led to either an increase or decrease in the production of various VOC classes, along with the specific compounds produced by Arabidopsis plants. In particular, ITCs (including 4-methylpentyl ITC and heptyl ITC) were only emitted from infested plants at 17 and 27°C, whereas they were not detected at 22°C. In contrast, certain VOC classes (such as sulfides [DMDS and DMTS] and nitrile [4-(methylthio) butanenitrile]) strongly increased in response to Arabidopsis plants that were infested at 22°C in comparison with plants maintained at 17 and 27°C after the 2 time intervals (Fig. 2 and Table 1). Several previous studies found that nitriles and sulfides, but not ITCs, originating from damaged A. thaliana may be detected in the gut of P. rapae, following infestation at 22 and 23°C.^22,26,43 It has been stated that P. rapae converts ITCs to nitriles through sulfatase activity.⁸ The myrosinase mediated GS degradation and formation of related volatile by-products can vary depending on the plants, cell pH, cell iron concentration, and temperature.^44-47 For instance, Williams et al.⁴⁷ indicated that increasing temperature is in favors of nitrile production in Lepidium sativum. For Arabidopsis, Van Poecke⁸ documented that the degradation of GSs leads to the production of either ITC or sulfide and nitrile compounds, depending on the activity of ethiospecifier modifier1 (ESM1) and ethiospecifier protein (ESP), respectively. Burow et al.⁴⁸ proved that the overexpression of ESP leads to nitrile production from ITCs in Arabidopsis plants upon larval (Spodoptera littoralis) infestation. In addition, there is also evidence of temperature affecting the activity of ESP.^49,50 For example, heat treatment causes ESP activity to decline in broccoli (Brassica oleracea var. italica).⁵⁰ Taken together, the production of GS derivative VOCs depended on the structure of GSs and reaction conditions. Wittstock and Burow⁴⁶ noted that the infestation of P. rapae on Arabidopsis plants caused a 2.fold8- induction of ESP transcription. In the present study, an increase or decrease in temperature may have had an immediate influence on the liberation of GS derivative volatiles from plants. Jin et al.⁵¹ indicated that a 5°C rise in the growth temperature range (21–23°C) leads to changes in the functional traits, structure, and biochemistry of A. thaliana leaves.

Many authors observed variations in the terpene emissions from plants exposed to different temperatures or herbivorous infestation.^2,10,20,52 Van Poecke et al.²² found that the AtTPS10 gene involved in terpene production is induced by P. rapae feeding on Arabidopsis plants. Herde et al.⁵³ found that P. xylostella larval infestation of Arabidopsis led the plant to emit (E,E)-α-farnesene and the C16-homoterpene TMTT ((E,E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene). In this study, we found that the emission of terpenes (including limonene, menthol, and (E,E)-α-farnesene) was influenced by the impact of both single factor (certain temperatures or larval infestation) and combined factor treatments (temperature and herbivore action combined) on Arabidopsis plants (Table 1). Pare and Tumlinson⁵⁴ reviewed that the emission of farnesene increased from insects-infested plant profiles in comparison with uninfested plants. In a previous study, Gouinguené and Turlings¹⁹ found that temperatures between 22 and 27°C caused higher emissions of certain terpenes (e.g., (E,E)-α-farnesene and (3E)-4,8-dimethyl-1,3,7-nonatriene [DMNT]) by Z. mays plants compared to lower and higher temperatures. It has been proposed that a change in temperature may influence the enzymatic reactions in the MEP pathways leading to altered terpene production.²

Like the study by Van Poecke et al.²² on caterpillar-Arabidopsis interactions, we found that pent-1-en-3-ol and 2-ethylhexan-1-ol were present in the volatile blends of Arabidopsis plants uninfested and infested by P. xylostella larvae at different temperatures (Table 1). Moreover, we also observed that the emission of certain aldehydes (2-ethylhexanal and benzaldehyde) and ketones (heptan-2-one, cyclohexanone, 6-methyl hept-5-en-2-one, octan-2-one, nonan-2-one, and geranyl acetone) changed with the temperature treatments in the presence or absence of larvae (Table 1). Most of these compounds were also found in the profiles of Arabidopsis volatiles by Rohloff and Bones.⁵⁵ It has also been suggested that the production of alcohols might change depending on the extent of stomatal opening and closure at different temperatures.^2,56,57 Filella et al.⁵⁸ found an increase of VOC emissions from Norway spruce (Picea abies) in response to rising temperature from 24 to 30°C.

It has been reported that in Arabidopsis infested by P. rapae, AtPAL1, which encodes phenylalanine ammonia-lyase, is correlated with the emission of MeSA via the phenylpropanoid pathway.^8,22 In our study, infestation with P. xylostella larvae caused Arabidopsis plants to release MeSA, with its relative abundance in chemical profiles being influenced by temperature treatments after the 2 time intervals (Table 1). A review by Loreto and Schnitzler² reported that temperature may have an important role in the release of plant MeSA. Some studies have found that the induction of MeSA in walnut plants (Paradox Hybrid; Juglans californica x J. regia) is associated with changes in temperature between day and night.^2,59

In conclusion, changes in temperature and P. xylostella larvae stress treatments caused significant changes in the volatile blends emitted by 5-week-old A. thaliana plantlets over 2 time intervals (0–4 and 4–8 h). In particular, the profiles of volatiles from diamondback moth larvae-infested plants varied with infestation time and temperature treatment (Fig. 1 and 2). The combination between temperature and pest larval infestation led to the emission of more VOCs compared to various temperature treatments alone (Table 1). Abiotic stresses (like cold, heat, and drought) relate to the expression of AT-00120 in the genome according to the Arabidopsis microarray database and the analysis toolbox sets using the Genevestigator tool (https://www.genevestigator.com/).^60,61 Thus, research focus is required on gene and protein expression related to VOC production from plants subjected to the change of abiotic and biotic factors. This approach could provide a potential way of elucidating the mechanisms of VOC production.

Materials and Methods

Plant material and growth conditions

All of the experimental procedures were performed with 5 week-old A. thaliana (L.) Heynh (ecotype Columbia [Col-0]). Seeds, supplied by Lehle Company (Texas, USA), were individually sown in plastic pots (0.20 l) with potting soil, and were stratified for 3 d at 4°C in the dark before being transferred in a growth chamber (21.8 ± 0.5°C). After germination, the seedlings were grown at 21.8 ± 0.5°C, 16L:8D (LED lighting: 43 μmol m⁻² s⁻¹ photosynthetically active radiation during the light period) and 66.2 ± 1.7% relative humidity (RH). The plants were watered twice a week (tap water, 10–20 ml/pot) for 5 weeks.

Insect rearing

Diamondback moth, P. xylostella (L.), larvae (2^nd–3^rd instar) were used in this study. Butterflies were kept in insect cages in a controlled temperature room, at 22 ± 2°C under a 16L:8D light regime and 50–70% RH. To maintain the P. xylostella population, pupae were collected, transferred to a gauze cage, and provided with 15% sugar solution as food source in a climate room. Eggs laid by the butterflies obtained from field were grown on cabbage plants (Brassica oleracea L.) until hatching into larvae.

Experimental device for VOC collection

Five-week-old Arabidopsis plants (9–10 leaves, 0.25–0.40 g/plant) were removed from the plastic pots, and the roots and soil were carefully wrapped in aluminum foil. Three plants were carefully placed together in a reaction vessel (100 ml, Duran Group, Germany) and subjected to each stress treatment. Prior to the onset of the experiments, reaction vessels were carefully cleaned with methanol and milli-Q water, and were then placed in the oven at 180°C for 24 h.

Influence of temperature treatments in the presence and absence of P. xylostella larvae on A. thaliana volatile emissions

Nine P. xylostella larvae were placed on each herbivore-treated Arabidopsis plant at different temperatures (17, 22, and 27°C) over the 2 time intervals (0–4 and 4–8 h). The larval density used in this study was chosen according to the observed VOC diversity that we found in the preliminary trials. In some previous studies on the effects of P. rapae and P. xylostella larvae on the defense responses of A. thaliana, similar larval densities were selected.^22,62

Arabidopsis plants (5 week-old) were assigned to 3 different temperature regimes: 17, 22, and 27°C in the presence and absence of 9 P. xylostella larvae. Temperature treatments were carried out with a thermostat water bath (IKA®-Werke GmbH & Co. KG, Germany), and the reaction vessels containing the 3 plants were plunged into the water and kept up to the end of each experimental condition (8 h). The temperature inside the collection reaction vessels was monitored by using a HOBO Pro temp/RH/light/text channel data logger (Onset Computer Corp., Bourne, MA 02532, USA). The same light intensity was maintained during all collections (600–800 Lux, HOBO Pro temp/RH/light/text channel data logger).

The experimentation related to VOC analyses was performed on 3 batches of culture at different moments. For each batch, 3 plants were randomly sampled after 5 weeks of cultivation.

Headspace VOC collection and GC-MS volatile analysis

Headspace solid phase microextraction (HS-SPME) technique has been used in many studies for profiling and characterization of VOCs from plants.^10,55,36-71

Similarly to our recent study on the effect of temperature–aphid interactions on Arabidopsis volatile emission,⁴² HS-SPME using the PDMS/DVB (65 μm) fiber (Supelo, Bellefonte, PA, USA) was selected. The choice of fiber was based on the results (data not shown) of preliminary experiments with different SPME fibers: polydimethylsiloxane–carboxen (PDMS/CAR, 75 μm), PDMS/DVB (65 μm), and polydimethylsiloxane–divinylbenzene–carboxen (PDMS/DVB/CAR, 50/30 μm) (Supelco, Bellefonte, PA, USA). Our results were in agreement with Rohloff and Bones.⁵⁵ The VOC sampling by SPME started at the beginning of each experimental treatment and was performed during 2 successive periods of 4 h each (0–4 and 4–8 h). Prior to the onset of VOC collection, the PDMS/DVB fibers were conditioned at 225°C for 30 min. Volatile collection was conducted across 2 time intervals (0–4 and 4–8 h).

At the end of the sampling periods (4 and 8 h), the fibers were desorbed in the splitless injector (220°C) of a gas chromatograph (Trace GC Ultra) coupled to a quadrupole-type mass spectrometer Trace Finnigan (Thermo-Fisher Scientific; Waltham, MA, USA). The GC was equipped with an apolar column (30 m; 0.25 mm i.d; 0.25 μm film thickness, Optima-5-MS, from Macherey-Nagel, Düren, Germany). The oven temperature program was: from 40 to 220°C (with 1-min final hold) at 4°C min⁻¹, and then from 220 to 320°C (10-min hold) at 100°C min⁻¹. Blank samples were regularly conducted to check possible carry over and peaks originating from the fibers. After each sampling, the fibers were immediately inserted into the GC injector for 5 min at 220°C to prevent contaminations. Helium was used as the carrier gas (constant flow rate of 1.5 ml min⁻¹). The mass spectra were obtained with a mass selective detector operating in electron ionization mode at 70 eV with a multiplier voltage of 275 V and a scanned mass range from 39 to 400 amu at a rate of 1 scan s⁻¹. The transfer line and ion source temperatures were maintained at 230°C and 250°C, respectively.

Chemical identification

Detected VOCs were identified based on their retention data and by careful examination of their mass spectra in comparison with the Wiley and NIST MS 2.0 mass spectral databases. Further identification was performed by comparison the retention time of the detected VOC peaks with those of the commercial compounds (provided by Sigma-Aldrich, Germany) analyzed under the same experimental conditions. The identification of VOCs was also carried out by comparing their calculated Retention index with the literature.

Statistical analyses

The relative abundance of individual VOCs was expressed as the ratio between their peak area and the total area of all detected VOCs from Arabidopsis plants exposed to each treatment. In a second step, the proportions of the VOC classes (terpenes, sulfides, nitrile, ketones, alcohols, aldehydes, ITCs, and ester) were calculated.

To determine the patterns and clusters between the volatile blends emitted by A. thaliana subjected to biotic and abiotic factors, PCA followed by a hierarchical clustering analysis (HCA) was performed using R 3.0.3 software,⁷² and the package FactoMineR 1.25.⁷³ PCA was performed on a dataset containing the relative abundance of either the individual compounds or the VOC classes for each experimental treatment, and the PCs were calculated using a correlation matrix. HCA was performed on an Euclidean distance matrix constructed from a data set containing the mean values of each experimental treatment on all PCs. From the calculated distance matrix, a hierarchical tree was constructed using the Ward algorithm and the hclust function of R 3.0.3.⁷²

Three-way ANOVA, and subsequent post hoc Tukey's tests, were used to compare the mean relative abundances of the individual VOCs, as well as the relative proportions of the VOC chemical families emitted by plants subjected to different treatments after 2 time intervals. For each subset, the log(× + 1) transformation of data was carried out when necessary, to meet assumptions of normality and homogeneity of variances. These tests were performed with Minitab® 16.2.2 software (State College, Pennsylvania, USA).

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.

Acknowledgments

The authors are grateful to Dr. Ian Dublon (Evolutionary Ecology and Genetics Group, Earth and Life Institute, Université catholique de Louvain) for his helpful collaboration.

Funding

Dieu-Hien Truong is the recipient of a Ph.D. scholarship from the Ministry of Education and Training Vietnam. Benjamin M. Delory received financial support from the Belgian Fund for Scientific Research (FRS-FNRS).

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PERMALINK

Plutella xylostella (L.) infestations at varying temperatures induce the emission of specific volatile blends by Arabidopsis thaliana (L.) Heynh

Dieu-Hien Truong

Benjamin M Delory

Yves Brostaux

Stéphanie Heuskin

Pierre Delaplace

Frédéric Francis

Georges Lognay

Abstract

Introduction

Results

Table 1.

Figure 1.

Figure 2.

Discussion

Materials and Methods

Plant material and growth conditions

Insect rearing

Experimental device for VOC collection

Influence of temperature treatments in the presence and absence of P. xylostella larvae on A. thaliana volatile emissions

Headspace VOC collection and GC-MS volatile analysis

Chemical identification

Statistical analyses

Disclosure of Potential Conflicts of Interest

Acknowledgments

Funding

References

ACTIONS

PERMALINK

RESOURCES

Cite

Add to Collections

PERMALINK

Plutella xylostella (L.) infestations at varying temperatures induce the emission of specific volatile blends by Arabidopsis thaliana (L.) Heynh

Dieu-Hien Truong

Benjamin M Delory

Yves Brostaux

Stéphanie Heuskin

Pierre Delaplace

Frédéric Francis

Georges Lognay

Abstract

Introduction

Results

Table 1.

Figure 1.

Figure 2.

Discussion

Materials and Methods

Plant material and growth conditions

Insect rearing

Experimental device for VOC collection

Influence of temperature treatments in the presence and absence of P. xylostella larvae on A. thaliana volatile emissions

Headspace VOC collection and GC-MS volatile analysis

Chemical identification

Statistical analyses

Disclosure of Potential Conflicts of Interest

Acknowledgments

Funding

References

ACTIONS

PERMALINK

RESOURCES

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