Effects of aphid herbivory on volatile organic compounds of Artemisia annua and Chrysanthemum morifolium

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Highlights

  • HS-SPME was used for volatile organic compounds collection.

  • Combined with the GC–MS data and olfactometer bioassay results.

  • Found two potential volatile compound to resist aphids.

Abstract

We showed the effect of aphid infesting on the volatile organic compounds (VOCs) emitted by the infested Artemisia annua and Chrysanthemum morifolium cultivar ‘Nan nong hong feng’ plants by using headspace solid-phase microextraction (HS-SPME) method combined with gas chromatography mass spectrometry (GC–MS). In olfactometer bioassay experiment, aphids showed a preference for the odour of both healthy and infested chrysanthemum, while we found an opposite result in A. annua. Aphids tend to healthy plants compared with the infested, and the phenomenon became obvious with time. Different extracts were tested with the healthy plants and aphid infested plants. Eucalyptol, β-caryophyllene, (E)-β-farnesene, and germacrene D were released as the major constituents in both species. After aphid infesting, we observed a great increase in artemisia ketone and (E)-β-farnesene and a decrease in germacrene D in A. annua; comparatively, eucalyptol, isoborneol and β-caryophyllene increased in chrysanthemum. Combined with the GC–MS data and olfactometer bioassay results we concluded that (E)-β-farnesene and artemisia ketone emitted from A. annua might act as a potential volatile compound to resist aphids, and the two compounds would be useful for future ecological control of aphid in chrysanthemum cultivation.

Introduction

Plants are famous for their ability to produce a diversity of secondary metabolites. They make and store a wide range of VOCs in flowers, leaves, fruits, and roots, where compounds are prepared and stored to be released into the surrounding atmosphere immediately upon an attack (Hegde et al., 2012). This response system can be a constitutive defense. Upon insect herbivory, plants can release blends of VOCs that against herbivory (Estell et al., 2013). Herbs sage (Salvia officinalis L.) and thyme (Thymus vulgaris L.) planted as intercrops among the crop plants Brussels sprouts (Brassica oleracea gemmifera L.) could significantly reduce oviposition of diamond-back moth (Plutella xylostella L.) (De Moraes et al., 2001, Dover, 1986). Hexane and ethanolic extracts from Dittrichia viscosa and Ferula communis were found against Spodoptera littoralis and Myzus persicae (Mamoci et al., 2012, Hegde et al., 2011). After aphid herbivory, the release of herbivore-induced plant volatiles (HIPVs) may get a repellent effect on aphids (Babikova et al., 2014). Behavioral test showed that cotton aphid (Aphis gossypii) was attracted to the odors from uninfested cotton plants but was repelled by odors from the infested plants (Hegde et al., 2011). HIPVs also play an important role in attracting natural enemies of aphids include predators and parasitoids, it would be helping the natural enemies identify and locate the prey of aphids (Hare, 2011). These HIPVs mainly comprise terpenoids, phenylpropanoids, benzenoid, fatty acid derivatives, green leaf volatiles (GLVs) and branched-chain amino acids (Dudareva et al., 2013). HIPVs mediate important interactions between plants and their environment are currently the most studied VOCs in the field of chemical ecology (Dicke, 2009, Huang et al., 2012). Nicotiana attenuata plants may release particular volatiles as a chemical signal to attract nature enemies to locating their prey on herbivore-attacked plants for defensive purposes (Halitschke et al., 2008). Moreover, recent research shows that HIPVs can serve as airborne signals in communication with plants nearby as indirect defenses, inducing and priming defenses in neighboring tissues and plants which was undamaged (Girón-Calva et al., 2012).

Chrysanthemum (Chrysanthemum morifolium), which belongs to the tribe Anthemideae in the Asteraceae family, is a traditional famous flower in China and the second most important cut flower in the world just after rose, with great ornamental and economic value (Teixeira da Silva et al., 2013). In commercial plantings especially in greenhouse, chrysanthemum is particularly susceptible to infestation by aphid (Macrosiphoniella sanbourni), a major pest throughout the world (Wang et al., 2014). The aphids are responsible for several damages to crop plant species as a result of mechanical injury, sap taking and virus vectors. In chrysanthemum production, aphids are currently controlled by chemical pesticides. The chemical control, however, has proven to be ineffective because of the increase in pesticide resistance and aphids remaining out of the reach. Moreover, the use of agrochemicals is associated with high cost and risks of environment and health (Qi et al., 2013). By contrast, the use of resistant cultivars is an economical, effective, and environmentally sound tactic to protect plants from insects while minimizing the use of insecticides. Previous researches reported some wild species carrying stress-resistant ability that is in absence in cultivar, which endowing opportunity of breeding resistant cultivars (Deng et al., 2010). Genus Artemisia belongs to the tribe Anthemideae in the Asteraceae family which gets close phylogenetic relationship with chrysanthemum, and it was reported get resistance to pests, disease and abiotic stress tolerance, because of its highly expression of bioactive secondary metabolites include monoterpenoids and sesquiterpenoids compounds (Deng et al., 2012, Negahban et al., 2007).

In the present study, we characterized the potential volatile compounds resulting in different aphid resistance between Artemisia annua and C. morifolium by investigating HIPVs emission of the two species after aphid herbivory under laboratory conditions through Headspace Solid-phase Microextraction (HS-SPME) method combined with Gas Chromatography-Mass Spectrometry (GC–MS), and by testing the responses of aphid to odors from the host food plants and clean air via wind tunnel bioassays. The findings provided an important implication for future ecological control of aphids in chrysanthemum cultivation.

Section snippets

Plant and aphid rearing

A. annua and chrysanthemum cultivar ‘Nan nong hong feng’ (maintained at the Chrysanthemum Germplasm Resource Preserving Centre, Nanjing Agricultural University, China) were cultivated in a greenhouse at 25 °C for 16 h daylight and 20 °C for 8 h darkness. After germination, plants were transplanted in 15 cm plastic pots including a mixture of vermiculite, peat, and perlite (1:1:1). Plants were grown to the 6–8 leaf stage before choosing a set of morphologically uniform seedlings.

Y-tube olfactometer bioassay

Olfactometer proved to be a suitable laboratory device for testing the orientation of the insects in complex odorous environments. Y-tube olfactometer bioassay showed that aphid had a preference for the odour of both healthy and treated chrysanthemum plants when tested against clean air (Table S1), and the result statistically significant for healthy chrysanthemum (P < 0.001, Fig. 1A). According to the results we may see a phenomenon that with the passage of time, the number of aphids attracted

Discussion

At present, no literature is available on the characterization of VOCs of aphid damaged A. annua or chrysanthemum, though the essential oil composition and VOCs were generally investigated in these two species (Haouas et al., 2012, Reale et al., 2011). In the present study, we characterized the changes in VOCs of A. annua and chrysanthemum when damaged by phloem-feeding aphids by using HS-SPME and GC–MS under laboratory conditions, and substantial VOCs were induced by aphid infestation. HIPVs

Acknowledgment

We thank Shanshan Wang and Yuxia Yang for assistance during collection of VOCs, Tao Wu for technical assistance for GC–MS standard.

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