The significance of antioxidants in the aphid‐plant interaction: the redox hypothesis

Abstract

The hypothesis is advanced that a redox system controls oxidation rates during the responses of plants to attack by sucking insects, that soluble antioxidants, such as ascorbate and glutathione, enhance the effectiveness of the plant's defensive system, and that oxidising enzymes in the saliva of aphids (and other phytophagous sucking insects) serve to counter it.Plants typically respond to wounding, including that caused by sucking insects, by mobilising and oxidising phenolic compounds. The initial phenolic monomers, and especially the monomeric o-quinones to which many give rise on oxidation, are generally deterrent to insects. Their final oxidation products, however, are polymers and phenol-protein conjugates, which are non-toxic, but serve to seal off damaged cells. It is suggested that effective defence by the plant requires oxidation of phenolics at a controlled rate that maintains a deterrent titre of the monomers, while allowing a well ordered deposition of sealants. It is also suggested that the salivary oxidases of the insects hasten oxidation in the affected tissues, thereby decreasing concentrations of monomeric phenols and quinones. It is further suggested that sedentary species may also thereby disorganise the sealing off of affected tissues.A kinetic model is developed to show that inclusion of a reductive cycle in the sequential oxidation of phenolics increases the steady state concentrations of monomeric phenols for a given throughput. Conversely, an increase in oxidation rates diminishes the titre of monomers for the same throughput.In initial biological tests of the hypothesis, infiltration of stems of lucerne cultivars with ascorbate or glutathione reduced the reproductive rate of spotted alfalfa aphid, Therioaphis trifolii maculata (Buckton), and of blue-green aphid, Acyrthosiphon kondo Shinji, feeding thereon. Intrinsically non-deterrent concentrations of ascorbate synergised the deterrence of the plant phenolics chlorogenic acid and catechin to the apple aphid, Aphis pomi (de Geer), and the spotted alfalfa aphid, T. t. maculata, respectively.

Oxidative Responses of Resistant and Susceptible Cereal Leaves to Symptomatic and Nonsymptomatic Cereal Aphid (Hemiptera: Aphididae) Feeding

“…Such contrasting differences between D. noxia-resistant Halt wheat and D. noxiasusceptible Morex barley may be the result of genetic differences in their metabolic pathways to scavenge oxidative radicals. The interruption of the balance of reduction and oxidation functions (i.e., redox system) in plants against sap-feeding insects has been designated as "the redox hypothesis" in aphidÐplant interactions (Miles and Oertli 1993). Although Miles and Oertli (1993) suggest that the change of oxidative activities is a natural part of plant defense against insect herbivory, the Þndings of our current study using the chlorosis-eliciting D. noxia and the nonchlorosis-eliciting R. padi indicate that cereal plant resistance against the aphid feeding might be complicated biochemical processes that need to be further examined.…”

“…The interruption of the balance of reduction and oxidation functions (i.e., redox system) in plants against sap-feeding insects has been designated as "the redox hypothesis" in aphidÐplant interactions (Miles and Oertli 1993). Although Miles and Oertli (1993) suggest that the change of oxidative activities is a natural part of plant defense against insect herbivory, the Þndings of our current study using the chlorosis-eliciting D. noxia and the nonchlorosis-eliciting R. padi indicate that cereal plant resistance against the aphid feeding might be complicated biochemical processes that need to be further examined. The results from this experiment will serve as the baseline information for us to understand the proteins involved in the defensive responses of plants to sapfeeding herbivores, and to ultimately identify enzymatic marker(s) for the screening of plant germplasms for herbivore resistance.…”

Categories of Resistance to Greenbug (Homoptera: Aphididae) Biotype I in <B> <I>Aegilops tauschii</I> </B> Germplasm

“…The watery saliva is suggested to contain various enzymes, including pectinases, cellulases, polyphenol oxidases, peroxidases, and lipases (Campbell and Dreyer 1990;Miles, 1990Miles, , 1999. These enzymes may perform vital roles in insect feeding, including lubrication of the stylets, maintaining favorable oxidative-reduction (redox) conditions and detoxification of phenolics and other chemical factors (Miles and Oertli, 1993). Furthermore, once the aphid reaches the sieve elements of the plant, salivary secretions help to limit phloem sealing and callose deposition, which enables the aphid to feed continuously for many hours or even days from a single sieve element (Will and van Bel, 2006;Will et al, 2007Will et al, , 2009.…”

Molecular sabotage of plant defense by aphid saliva

“…Indeed, it has frequently been hypothesized that the watery saliva interferes with the sieve plate occlusion mechanisms in response to penetration of the SE (16,20,23,24). One way that watery saliva could interfere with sieve plate occlusion would be to bind calcium in the SE and thus prevent calcium from exceeding a threshold level (25) that would trigger SE occlusion.…”