Metabolic fate of the allelochemical nicotine in the tobacco hornworm Manduca sexta

Snyder, Mark J.; Walding, Jennifer K.; Feyereisen, René

doi:10.1016/0965-1748(94)90112-0

Cited by 62 publications

(50 citation statements)

References 25 publications

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“…Although the CYPs have been mainly thought to mediate the oxidation of nicotine (11,14), none of the nicotine oxides were detected in hemolymph, frass, excised guts, and larval headspace of WT-fed and CYP-silenced larvae [which is consistent with the findings of Self et al (17)]. Thus, it is possible that instead of producing these stable nicotine oxides, midgut-based CYP6B46 may convert nicotine to a short-lived metabolite that is readily pumped to the hemolymph and reconverts to nicotine immediately on entering the hemolymph, as originally proposed by Morris (38).…”

Section: Discussionmentioning

confidence: 99%

“…on the polar metabolites of nicotine, such as cotinine and the N-oxides of both nicotine and cotinine, which are commonly found in the urine and blood of human smokers (8,11,12); cytochrome P450s (CYPs) are thought to mediate nicotine's oxidation to these metabolites (8,11,(13)(14)(15), but other researchers have been unable to find the oxides in M. sexta's excretions and propose that nicotine is rapidly excreted without modification (16)(17)(18). Although this theory is widely accepted, most studies have not been able to recover all of the ingested nicotine in the frass and nicotine can be found in the hemolymph of larvae feeding on nicotine-containing diets.…”

Section: Significancementioning

confidence: 99%

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Natural history-driven, plant-mediated RNAi-based study reveals CYP6B46 ’s role in a nicotine-mediated antipredator herbivore defense

Kumar

Pandit

Steppuhn

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

118

119

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Significance When hornworm ( Manduca sexta ) larvae feed on Nicotiana attenuata plants in native habitats, more disappear at night when they feed on transgenic, nicotine-free N. attenuata plants because wolf spiders ( Camptocosa parallela ) selectively prey on nicotine-free larvae. When larvae consume nicotine-replete plants, their midgut-expressed cytochrome P450 6B46 ( CYP6B46 ) is upregulated. The larvae in which CYP6B46 is silenced by plant-mediated RNAi excrete more of their ingested nicotine. Silencing CYP6B46 impairs the mechanisms of passing ingested nicotine from the midgut to the hemolymph to be exhaled from the spiracles during spider attack. Spiders are deterred by this nicotine-rich halitosis. Thus, the CYP6B46 -silenced larvae exhale less nicotine and become ready spider prey, demonstrating that CYP6B46 functions to repurpose the normally excreted nicotine for defense.

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Section: Discussionmentioning

confidence: 99%

Section: Significancementioning

confidence: 99%

Natural history-driven, plant-mediated RNAi-based study reveals CYP6B46 ’s role in a nicotine-mediated antipredator herbivore defense

Kumar

Pandit

Steppuhn

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

118

119

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“…Mark Snyder and I discovered that M. sexta can override this aversive response by repeatedly sampling a nicotine diet over a period of 30 h. As a result of this sampling behavior, specialized cells in the wall of the midgut gradually induce large quantities of P450 detoxication enzymes (Figures 8a-d). These P450 enzymes catabolize nicotine into less toxic and excretable metabolites (Snyder et al, 1993(Snyder et al, , 1994. Two lines of evidence support a causal connection between the induction of P450 enzymes and the disappearance of the aversive response to nicotine.…”

Section: Mechanisms For Overriding the Aversive Responsementioning

confidence: 94%

How do herbivorous insects cope with noxious secondary plant compounds in their diet?

Glendinning

2002

Entomologia Exp Applicata

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Herbivorous insects use a variety of physiological mechanisms to cope with noxious (i.e., unpalatable and/or toxic) compounds in their food plants. Here, I review what is known about this coping process, focusing on one species of caterpillar, the tobacco hornworm (Manduca sexta). Herbivorous insects possess both preingestive (i.e., chemosensory) and postingestive response mechanisms for detecting plant secondary compounds. Stimulation of either class of detection mechanism inhibits feeding rapidly by reducing biting rate and/or bite size. This aversive response is highly adaptive during encounters with secondary plant compounds that are toxic. The insect's dilemma is that many harmless or mildly toxic compounds also activate the aversive response. To overcome this dilemma, herbivorous insects employ at least three mechanisms for selectively deactivating their aversive response to relatively harmless secondary plant compounds: (1) the presence of carbohydrates can mask the unpalatable taste of some secondary plant compounds; (2) prolonged dietary exposure to some unpalatable secondary plant compounds can initiate long-term adaptation mechanisms in the peripheral and central gustatory system; and (3) dietary exposure to toxic compounds can induce production of P450 detoxication enzymes. Thus, herbivorous insects utilize an integrated suite of physiological mechanisms to detect potentially toxic compounds in foods, and then selectively adapt to those that do not pose a serious threat to their growth and survivorship.

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“…*, Significantly different values from pTV00 with P , 0.05. negative effects on larval growth. Moreover, hornworm tolerates doses of nicotine that unadapted insects find fatal (Snyder et al, 1994), and it is possible that other primary metabolites, such as proteins or carbohydrate levels altered by the VIGS system, may have minimized the influence of nicotine and TPIs on larval growth. Low nitrogen (N) supply attenuated JAinduced TPI and nicotine levels in N. attenuata (Lou and Baldwin, 2004), which points to the importance of plant growth conditions in influencing defensive function of particular metabolites.…”

Section: Discussionmentioning

confidence: 99%

Silencing Geranylgeranyl Diphosphate Synthase inNicotiana attenuataDramatically Impairs Resistance to Tobacco Hornworm

et al. 2007

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In bioassays with artificial diets, the 17-hydroxygeranyllinalool diterpenoid glycosides (HGL-DTGs) of Nicotiana attenuata function as antifeedants for the plant's adapted herbivore, tobacco hornworm (Manduca sexta). To determine whether HGLDTGs have a defensive function in planta, we suppressed HGL-DTG production by silencing the source of the geranylgeranyl diphosphates (GGPPs) required for geranyllinalool biosynthesis, a key intermediate. We used virus-induced gene silencing to suppress transcript levels of GGPP synthase gene (Naggpps) and farnesyl diphosphate (FPP) synthase gene (Nafpps), northern blotting and real-time polymerase chain reaction to quantify transcript accumulations, and radio gas chromatography to analyze prenyltransferase specificity. Silencing Nafpps had no effect on the accumulation of HGL-DTGs but decreased leaf steroid content, demonstrating that DTG-synthesizing enzymes do not use GGPP derived from FPP and confirming FPP's role as a steroid precursor. Unlike plants silenced in the phytoene desaturase gene (Napds), which rapidly bleached, Naggppssilenced plants had reduced HGL-DTG but not carotenoids or chlorophyll contents, demonstrating that Naggpps supplies substrates for GGPP biosynthesis for HGL-DTGs, but not for phytoene or phytol. Expression of Naggpps in Escherichia coli revealed that the recombinant protein catalyzes the GGPP synthesis from isopentenyl diphosphate and dimethylallyl diphosphate. When fed on silenced plants, hornworm larvae gained up to 3 times more mass than those that fed on empty vector control plants or plants silenced in Nafpps, the trypsin protease inhibitor gene, or the putrescine N-methyltransferase gene. We conclude that HGL-DTGs or other minor undetected diterpenoids derived from GGPP function as direct defenses for N. attenuata and are more potent than nicotine or trypsin protease inhibitors against attack by hornworm larvae.

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Metabolic fate of the allelochemical nicotine in the tobacco hornworm Manduca sexta

Cited by 62 publications

References 25 publications

Natural history-driven, plant-mediated RNAi-based study reveals CYP6B46 ’s role in a nicotine-mediated antipredator herbivore defense

Natural history-driven, plant-mediated RNAi-based study reveals CYP6B46 ’s role in a nicotine-mediated antipredator herbivore defense

How do herbivorous insects cope with noxious secondary plant compounds in their diet?

Silencing Geranylgeranyl Diphosphate Synthase inNicotiana attenuataDramatically Impairs Resistance to Tobacco Hornworm

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