The cabbage aphid: a walking mustard oil bomb

Abstract

The cabbage aphid, Brevicoryne brassicae, has developed a chemical defence system that exploits and mimics that of its host plants, involving sequestration of the major plant secondary metabolites (glucosinolates). Like its host plants, the aphid produces a myrosinase (b-thioglucoside glucohydrolase) to catalyse the hydrolysis of glucosinolates, yielding biologically active products. Here, we demonstrate that aphid myrosinase expression in head/thoracic muscle starts during embryonic development and protein levels continue to accumulate after the nymphs are born. However, aphids are entirely dependent on the host plant for the glucosinolate substrate, which they store in the haemolymph. Uptake of a glucosinolate (sinigrin) was investigated when aphids fed on plants or an in vitro system and followed a different developmental pattern in winged and wingless aphid morphs. In nymphs of the wingless aphid morph, glucosinolate level continued to increase throughout the development to the adult stage, but the quantity in nymphs of the winged form peaked before eclosion (at day 7) and subsequently declined. Winged aphids excreted significantly higher amounts of glucosinolate in the honeydew when compared with wingless aphids, suggesting regulated transport across the gut. The higher level of sinigrin in wingless aphids had a significant negative impact on survival of a ladybird predator. Larvae of Adalia bipunctata were unable to survive when fed adult wingless aphids from a 1% sinigrin diet, but survived successfully when fed aphids from a glucosinolate-free diet (wingless or winged), or winged aphids from 1% sinigrin. The apparent lack of an effective chemical defence system in adult winged aphids possibly reflects their energetic investment in flight as an alternative predator avoidance mechanism.

Phyllotreta striolataflea beetles use host plant defense compounds to create their own glucosinolate-myrosinase system

“…The mechanism by which the beetle controls the hydrolysis of its stored glucosinolates to avoid autointoxication remains to be determined but is likely to be actively controlled. In contrast, the "mustard-oil bomb" in aphids is activated when an individual is attacked by a predator, which benefits the survival of the clonal aphid colony by repelling the predator (17,19,47). Although we cannot rule out the participation of sequestered glucosinolates in a similar defense in Phyllotreta, an additional signaling role is also suggested by previous studies showing that ITCs enhance the response to the male-produced aggregation pheromone (26)(27)(28)(29).…”

“…sawflies show species-specific sequestration patterns in the hemolymph that were suggested to reflect adaptations to different host plants (16,38). In the crucifer aphid, B. brassicae, glucosinolate accumulation in the hemolymph differs quantitatively between wingless and winged morphs feeding on the same diet, which indicates regulated transport between the gut and hemolymph (17). We also assume that transporters are involved in glucosinolate uptake from the gut in P. striolata.…”

“…Although several generalist lepidopterans detoxify ITCs via conjugation with glutathione (10), the specialists investigated so far circumvent ITC formation (7,11,12). Several adapted herbivores sequester intact host plant glucosinolates (13-16), and two aphid species, Brevicoryne brassicae and Lipaphis erysimi, not only sequester glucosinolates but also convert these glucosinolates to toxic ITCs by using their own myrosinase, encoded in the aphid genome (17)(18)(19)(20).Flea beetles of the genus Phyllotreta (Coleoptera: Chrysomelidae) are closely associated with glucosinolate-containing plants in the Brassicaceae, Resedaceae, Tropaeolaceae, and Capparaceae on which they feed throughout their life cycle (21-23). In fact, the only confirmed exception is Phyllotreta vittula, which prefers Poaceae but also accepts crucifers as food plants (24).…”

“…Although several generalist lepidopterans detoxify ITCs via conjugation with glutathione (10), the specialists investigated so far circumvent ITC formation (7,11,12). Several adapted herbivores sequester intact host plant glucosinolates (13-16), and two aphid species, Brevicoryne brassicae and Lipaphis erysimi, not only sequester glucosinolates but also convert these glucosinolates to toxic ITCs by using their own myrosinase, encoded in the aphid genome (17)(18)(19)(20).…”

Formation of Simple Nitriles upon Glucosinolate Hydrolysis Affects Direct and Indirect Defense Against the Specialist Herbivore, Pieris rapae

“…A few studies have demonstrated that parasitoids are attracted to isothiocyanates (Titayavan and Altieri 1990;Pivnick 1993;Murchie et al 1997;Bradburne and Mithen 2000;Reddy et al 2002;Blande et al 2007). However, parasitoid and predator performance is also known to correlate negatively with glucosinolate content (Harvey et al 2003;Kazana et al 2007;Gols et al 2008). This negative relationship might favor a behavioral response of predators and parasitoids to plant volatiles that contain simple nitriles instead of isothiocyanates.…”