Host plants and obligate endosymbionts are not the sources for biosynthesis of the aphid alarm pheromone

Sun, Zhihong; Li, Zhengxi

doi:10.1038/s41598-017-06465-9

Cited by 13 publications

(19 citation statements)

References 57 publications

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“…The EβF content in the aphid was quantitatively measured after RNAi by using the method modified from Fischer and Lognay () and Francis et al (). Briefly, the emitters with secretion were put into 2 ml microcentrifuge tubes on the ice which contained 200 μl of distilled hexane and 0.2 μl decane (purity > 99.9%) as an internal standard for quantification by gas chromatography–mass spectrometry (Sun and Li, ). The non‐emitters were placed in 1.5 ml microcentrifuge tubes, and both emitters and non‐emitters were weighed on an electronic analytical balance (A200S, 0.0001 g, Sartorius) for calculating the concentration of EβF per milligram of aphid.…”

Section: Methodsmentioning

confidence: 99%

“…These facts prompted us to speculate that there are other sources than aphids themselves responsible for EβF biosynthesis, especially the host plant and endosymbionts of aphids. However, we have recently eliminated the possibility of the host plant and endosymbionts as the sources of the EβF released by aphids by rearing aphids on nonplant artificial diets and by antibiotic treatment respectively (Sun and Li, ). It is therefore most likely that the aphid itself is responsible for EβF biosynthesis.…”

Section: Introductionmentioning

confidence: 99%

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The terpenoid backbone biosynthesis pathway directly affects the biosynthesis of alarm pheromone in the aphid

Sun

2018

Insect Molecular Biology

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The terpenoid backbone biosynthesis pathway is responsible for the synthesis of different backbones for terpenoids; (E)-β-farnesene (EβF), a sesquiterpene, is the major component of aphid alarm pheromone. Our previous studies eliminated the possibility of host plants and endosymbionts as the sources of EβF, and we thus speculate that the terpenoid pathway might affect the biosynthesis of EβF in aphids. First, the transcriptional responses of four genes encoding farnesyl diphosphate synthase (FPPS), geranylgeranyl diphosphate synthase (GGPPS) and decaprenyl diphosphate synthase in the cotton aphid Aphis gossypii to simulated stimulation were analysed using quantitative real-time PCR, showing an immediate decrease in the transcript abundances of the four genes. Next, RNA-interference-mediated gene knockdown was performed, indicating that fpps knockdown caused a significant cost in terms of body size and fecundity. Finally, an association analysis of gene knockdown with the amount of EβF was conducted, revealing that the concentration of EβF per milligram of aphid was drastically decreased in response to fpps knockdown, whereas ggpps knockdown significantly raised the concentration of EβF. Our data support a peculiar mode of biosynthesis and storage of the aphid alarm pheromone that relies directly on the terpenoid backbone biosynthesis pathway in the aphid.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The terpenoid backbone biosynthesis pathway directly affects the biosynthesis of alarm pheromone in the aphid

Sun

2018

Insect Molecular Biology

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“…Since then, many FPPS genes have been identified in other insects, including aphid species (Cusson et al ., 2006; Sen et al ., 2007; Lewis et al ., 2008; Taban et al ., 2009; Bomtorin et al ., 2014; Huang et al ., 2015). In our laboratory, we have worked on aphid FPPS genes for many years, including MpFPPS1 and MpFPPS2 in M. persicae (Zhang & Li, 2008, 2012), AgFPPS in the cotton aphid Aphis gossypii (Ma et al ., 2010; Zhang & Li, 2013, 2014; Sun & Li, 2017) and RpFPPS1 and RpFPPS2 in the bird cherry-oat aphid Rhopalosiphum padi (Sun & Li, 2012). In vitro analysis of enzymatic activity with recombinant proteins showed that aphid FPPSs displayed dual geranyl/FPPS activity, and a linked enzymatic assay using the aphid FPPS and peppermint sesquiterpene synthase produced EβF (Lewis et al ., 2008), indicating the potential involvement of aphid FPPS in the biosynthesis of alarm pheromone.…”

Section: Introductionmentioning

confidence: 99%

Spatiotemporal expression profiling of the farnesyl diphosphate synthase genes in aphids and analysis of their associations with the biosynthesis of alarm pheromone

Cheng

2018

Bull. Entomol. Res.

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The alarm behavior plays a key role in the ecology of aphids, but the site and molecular mechanism for the biosynthesis of aphid alarm pheromone are largely unknown. Farnesyl diphosphate synthase (FPPS) catalyzes the synthesis of FPP, providing the precursor for the alarm pheromone (E)-β-farnesene (EβF), and we speculate that FPPS is closely associated with the biosynthetic pathway of EβF. We firstly analyzed the spatiotemporal expression of FPPS genes by using quantitative reverse transcription-polymerase chain reaction, showing that they were expressed uninterruptedly from the embryonic stage to adult stage, with an obvious increasing trend from embryo to 4th-instar in the green peach aphid Myzus persicae, but FPPS1 had an overall significantly higher expression level than FPPS2; both FPPS1 and FPPS2 exhibited the highest expression in the cornicle area. This expression pattern was verified in Acyrthosiphon pisum, suggesting that FPPS1 may play a more important role in aphids and the cornicle area is most likely the site for EβF biosynthesis. We thus conducted a quantitative measurement of EβF in M. persicae by gas chromatography-mass spectrometry. The data obtained were used to perform an association analysis with the expression data, revealing that the content of EβF per aphid was significantly correlated with the mean weight per aphid (r = 0.8534, P = 0.0307) and the expression level of FPPS1 (r = 0.9134, P = 0.0109), but not with that of FPPS2 (r = 0.4113, P = 0.4179); the concentration of EβF per milligram of aphid was not correlated with the mean weight per aphid or the expression level of FPPS genes. These data suggest that FPPS1 may play a key role in the biosynthesis of aphid alarm pheromone.

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“…The artificial diet was prepared as previously described (Z. J. Sun & Li, ). Briefly, a two‐way glass tube (⌀3.0 cm) was used, with a 150‐µl diet sealed between two layers of aseptic parafilm at one end and with filter paper covering the other end to prevent aphids from escaping.…”

Section: Methodsmentioning

confidence: 99%

“…In fact, it is unclear if EβF released from the aphid is synthesized de novo; until recently, the possibility of the host plant and endosymbionts as the sources of EβF has been eliminated (Z. J. Sun & Li, ). Thus, it is postulated that EβF is synthesized by the aphid, but the molecular mechanism is largely unknown.…”

Section: Introductionmentioning

confidence: 99%

Both farnesyl diphosphate synthase genes are involved in the production of alarm pheromone in the green peach aphid Myzus persicae

Cheng

2018

Arch Insect Biochem Physiol

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Farnesyl diphosphate synthase (FPPS) catalyzes the formation of FPP, providing the precursor for the biosynthesis of (E)-βfarnesene (EβF) in plants, but it is unknown if FPPS supplies the precursor for the biosynthesis of EβF, the major component of aphid alarm pheromone, though our previous studies support the hypothesis that EβF is synthesized by the aphid itself. Here, we used two cohorts of the green peach aphid Myzus persicae separately, reared on pepper plant and artificial diet to test the correlations among droplet emission, EβF quantity, and FPPS gene expression. It was found that the proportion of aphids emitting cornicle droplets and the quantity of EβF per milligram of aphid were both significantly different between the two cohorts, which were positively correlated with the expression of the two FPPS genes (MpFPPS1/2) in M. persicae. These results were further confirmed by RNAi-mediated knockdown of MpFPPS1/2. Specifically, knockdown of MpFPPS1/2 imposed no significant cost on the survival of aphid but remarkably increased the number of offspring per aphid; most importantly, knockdown of MpFPPS1/2 significantly reduced the proportion of aphids emitting droplets and the quantity of EβF calculated as per the weight of aphid. Our results suggest that both FPPS genes are involved in the production of EβF in M. persicae and cornicle droplet emission is closely associated with the EβF release in the aphid. K E Y W O R D S (E)-β-farnesene, farnesyl diphosphate synthase, Myzus persicae, RNAi Arch. Insect Biochem. Physiol. 2019;100:e21530.wileyonlinelibrary.com/journal/arch

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Host plants and obligate endosymbionts are not the sources for biosynthesis of the aphid alarm pheromone

Cited by 13 publications

References 57 publications

The terpenoid backbone biosynthesis pathway directly affects the biosynthesis of alarm pheromone in the aphid

The terpenoid backbone biosynthesis pathway directly affects the biosynthesis of alarm pheromone in the aphid

Spatiotemporal expression profiling of the farnesyl diphosphate synthase genes in aphids and analysis of their associations with the biosynthesis of alarm pheromone

Both farnesyl diphosphate synthase genes are involved in the production of alarm pheromone in the green peach aphid Myzus persicae

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