Vitamin C content in plants is modified by insects and influences susceptibility to herbivory

Goggin, Fiona L.; Avila, Carlos A.; Lorence, Argelia

doi:10.1002/bies.200900187

Cited by 40 publications

(34 citation statements)

References 94 publications

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“…Ascorbate has multiple functions in animals and plants, including acting as an antioxidant, serving as a cofactor for various enzymes, and participating in cell signalling (Corti et al, 2010; Foyer and Noctor, 2011; Goggin et al, 2010; Pignocchi and Foyer, 2003). Ascorbate is present in animals and plants as ascorbate (reduced form), monodehydroascorbate (a radical that is formed after the loss of one electron), and dehydroascorbate (a somewhat more stable oxidized form that is created by the loss of two electrons).…”

Section: Discussionmentioning

confidence: 99%

Multicopper oxidase-1 orthologs from diverse insect species have ascorbate oxidase activity

Peng

Dittmer

Lang

et al. 2015

Insect Biochemistry and Molecular Biology

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Members of the multicopper oxidase (MCO) family of enzymes can be classified by their substrate specificity; for example, ferroxidases oxidize ferrous iron, ascorbate oxidases oxidize ascorbate, and laccases oxidize aromatic substrates such as diphenols. Our previous work on an insect multicopper oxidase, MCO1, suggested that it may function as a ferroxidase. This hypothesis was based on three lines of evidence: RNAi-mediated knock down of Drosophila melanogaster MCO1 (DmMCO1) affects iron homeostasis, DmMCO1 has ferroxidase activity, and DmMCO1 has predicted iron binding residues. In our current study, we expanded our focus to include MCO1 from Anopheles gambiae, Tribolium castaneum, and Manduca sexta. We verified that MCO1 orthologs have similar expression profiles, and that the MCO1 protein is located on the basal surface of cells where it is positioned to oxidize substrates in the hemolymph. In addition, we determined that RNAi-mediated knock down of MCO1 in A. gambiae affects iron homeostasis. To further characterize the enzymatic activity of MCO1 orthologs, we purified recombinant MCO1 from all four insect species and performed kinetic analyses using ferrous iron, ascorbate and two diphenols as substrates. We found that all of the MCO1 orthologs are much better at oxidizing ascorbate than they are at oxidizing ferrous iron or diphenols. This result is surpring because ascorbate oxidases are thought to be specific to plants and fungi. An analysis of three predicted iron binding residues in DmMCO1 revealed that they are not required for ferroxidase or laccase activity, but two of the residues (His374 and Asp380) influence oxidation of ascorbate. These two residues are conserved in MCO1 orthologs from insects and crustaceans; therefore, they are likely to be important for MCO1 function. The results of this study suggest that MCO1 orthologs function as ascorbate oxidases and influence iron homeostasis through an unknown mechanism.

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Section: Discussionmentioning

confidence: 99%

Multicopper oxidase-1 orthologs from diverse insect species have ascorbate oxidase activity

Peng

Dittmer

Lang

et al. 2015

Insect Biochemistry and Molecular Biology

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“…Although these results show significant promise for the development of plants with enhanced abiotic stress tolerance, elevated AsA content may affect the ability of plants to interact with insects and other herbivores (Goggin et al 2010). Fine regulation of these genes may allow the production of transgenic plants, with tolerances to a wide range of stresses.…”

Section: Discussionmentioning

confidence: 99%

Elevating vitamin C content via overexpression of myo-inositol oxygenase and l-gulono-1,4-lactone oxidase in Arabidopsis leads to enhanced biomass and tolerance to abiotic stresses

Lisko

Torres

Harris

et al. 2013

In Vitro Cell.Dev.Biol.-Plant

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l-Ascorbic acid (vitamin C) is an abundant metabolite in plant cells and tissues. Ascorbate functions as an antioxidant, as an enzyme cofactor, and plays essential roles in multiple physiological processes including photosynthesis, photoprotection, control of cell cycle and cell elongation, and modulation of flowering time, gene regulation, and senescence. The importance of this key molecule in regulating whole plant morphology, cell structure, and plant development has been clearly established via characterization of low vitamin C mutants of Arabidopsis, potato, tobacco, tomato, and rice. However, the consequences of elevating ascorbate content in plant growth and development are poorly understood. Here we demonstrate that Arabidopsis lines over-expressing a myo-inositol oxygenase or an l-gulono-1,4-lactone oxidase, containing elevated ascorbate, display enhanced growth and biomass accumulation of both aerial and root tissues. To our knowledge this is the first study demonstrating such a marked positive effect in plant growth in lines engineered to contain elevated vitamin C content. In addition, we present evidence showing that these lines are tolerant to a wide range of abiotic stresses including salt, cold, and heat. Total ascorbate content of the transgenic lines remained higher than those of controls under the abiotic stresses tested. Interestingly, exposure to pyrene, a polycyclic aromatic hydrocarbon and known inducer of oxidative stress in plants, leads to stunted growth of the aerial tissue, reduction in the number of root hairs, and inhibition of leaf expansion in wild type plants, while these symptoms are less severe in the over-expressers. Our results indicate the potential of this metabolic engineering strategy to develop crops with enhanced biomass, abiotic stress tolerance, and phytoremediation capabilities.

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“…One of the components of the plant antioxidant system is ascorbic acid (AsA) (Hancock & Viola, 2005). Several lines of research have previously suggested that AsA plays a key role in plant-insect interactions, as its abundance in plants modifies insect infestation ability and/or plant susceptibility to insect feeding (Goggin et al, 2010). Several mechanisms have been suggested by which AsA modulates insect success on plants: effects may be mediated by AsA as an essential dietary nutrient, as an antioxidant in the insect midgut neutralizing harmful H 2 O 2 , or as a substrate for plant-derived AsA oxidase, which can lead to generation of toxic ROS.…”

Section: Discussionmentioning

confidence: 99%

“…Several lines of research have previously suggested that AsA plays a key role in plant-insect interactions, as its abundance in plants modifies insect infestation ability and/or plant susceptibility to insect feeding (Goggin et al, 2010). Ascorbic acid can also influence the efficacy of plant defences such as myrosinases and tannins, and alter insects' susceptibility to natural enemies (Goggin et al, 2010). Ascorbic acid can also influence the efficacy of plant defences such as myrosinases and tannins, and alter insects' susceptibility to natural enemies (Goggin et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

“…On the contrary, opposite effects induced by a previous infestation, making the plant more attractive and/or susceptible to herbivory by the same species, were also observed (Prado & Tjallingii, 1997;Thaler et al, 2001). In turn, increasing evidence points to the involvement of reactive oxygen species (ROS) in the plant response to insect infestation (including aphids), and the hormone-mediated ability of the insects to bypass plant-defence responses (Kusnierczyk et al, 2008;Goggin et al, 2010). None of these defence mechanisms can successfully explain facilitation of a subsequent aphid attack after an earlier infestation.…”

Section: Introductionmentioning

confidence: 99%

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Impact of plant and aphid stress history on infestation in arugula plants

Menéndez

Folcia

Vizgarra

et al. 2013

Entomologia Exp Applicata

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Plants can activate inducible defence mechanisms against pests, pathogens, or chemical elicitors, such as ozone, mediated by reactive oxygen species (ROS), particularly hydrogen peroxide (H 2 O 2 ). An unfavourable balance between ROS production and the plant antioxidant capacity seems to be responsible for the resulting susceptibility of the plant to insect attack. Arugula plants [Eruca sativa Mill. (Brassicaceae)] and green peach aphids, Myzus persicae (Sulzer) (Hemiptera: Aphididae), were used in this study to test the hypothesis that the growth of an aphid population depends on both plant and insect stress history. We investigated the impact of density and duration of a previous aphid infestation, and the time lag before re-infestation, on aphid population growth. In a second experiment, we assessed the effect on aphid population growth of previous ozone exposure of arugula plants in open top chambers receiving a continuous O 3 fumigation of 100-120 p.p.b., 90 min per day during 3 days. A third experiment was conducted to study the effect of aphid density during a previous infestation on the population growth on an uninfested host. Both previous herbivory and ozone changed the oxidative status of plant tissues and facilitated aphid population growth, which increased with the duration and density of a previous infestation by aphids. Colonization success also depended on the aphids' own history. Aphids coming from high-density populations and/or longer infestation periods produced larger populations on an (initially) uninfested plant. Pest outbreaks in a polluted environment might be expected to be modulated by the hosts' spatial-temporal heterogeneity related to the ozone exposure and previous herbivory.

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Vitamin C content in plants is modified by insects and influences susceptibility to herbivory

Cited by 40 publications

References 94 publications

Multicopper oxidase-1 orthologs from diverse insect species have ascorbate oxidase activity

Multicopper oxidase-1 orthologs from diverse insect species have ascorbate oxidase activity

Elevating vitamin C content via overexpression of myo-inositol oxygenase and l-gulono-1,4-lactone oxidase in Arabidopsis leads to enhanced biomass and tolerance to abiotic stresses

Impact of plant and aphid stress history on infestation in arugula plants

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