Role of Large Cabbage White butterfly male-derived compounds in elicitation of direct and indirect egg-killing defenses in the black mustard

Abstract

To successfully exert defenses against herbivores and pathogens plants need to recognize reliable cues produced by their attackers. Up to now, few elicitors associated with herbivorous insects have been identified. We have previously shown that accessory reproductive gland secretions associated with eggs of Cabbage White butterflies (Pieris spp.) induce chemical changes in Brussels sprouts plants recruiting egg-killing parasitoids. Only secretions of mated female butterflies contain minute amounts of male-derived anti-aphrodisiac compounds that elicit this indirect plant defense. Here, we used the black mustard (Brassica nigra) to investigate how eggs of the Large Cabbage White butterfly (Pieris brassicae) induce, either an egg-killing direct [i.e., hypersensitive response (HR)-like necrosis] or indirect defense (i.e., oviposition-induced plant volatiles attracting Trichogramma egg parasitoids). Plants induced by P. brassicae egg-associated secretions expressed both traits and previous mating enhanced elicitation. Treatment with the anti-aphrodisiac compound of P. brassicae, benzyl cyanide (BC), induced stronger HR when compared to controls. Expression of the salicylic (SA) pathway- and HR-marker PATHOGENESIS-RELATED GENE1 was induced only in plants showing an HR-like necrosis. Trichogramma wasps were attracted to volatiles induced by secretion of mated P. brassicae females but application of BC did not elicit the parasitoid-attracting volatiles. We conclude that egg-associated secretions of Pieris butterflies contain specific elicitors of the different plant defense traits against eggs in Brassica plants. While in Brussels sprouts plants anti-aphrodisiac compounds in Pieris egg-associated secretions were clearly shown to elicit indirect defense, the wild relative B. nigra, recognizes different herbivore cues that mediate the defensive responses. These results add another level of specificity to the mechanisms by which plants recognize their attackers.

Juvenile Spider Mites Induce Salicylate Defenses, but Not Jasmonate Defenses, Unlike Adults

“…Mechanical injury is well known for eliciting repair and defense responses (Mithöfer et al, 2005;Duran-Flores and Heil, 2016). Second, plants may respond to spider mite egg-deposition as has been demonstrated for the eggs of dipteran (Hilker et al, 2002;Bittner et al, 2017), lepidopteran (Fatouros et al, 2015), and coleopteran (Doss et al, 2000) insects, and was shown to sometimes benefit the insect (Hilker and Fatouros, 2015;Hilker and Fatouros, 2016). Third, plants may respond to spider mite secretions such as silk (Grbic et al, 2011;Dogȃn et al, 2017), feces (Santamaria et al, 2015), and especially the saliva they inject into host cells during feeding, reminiscent of herbivorous insects (Howe and Jander, 2008;Maffei et al, 2012).…”

Arabidopsis, tobacco, nightshade and elm take insect eggs as herbivore alarm and show similar transcriptomic alarm responses

“… 28 – 30 . PR genes are also more strongly expressed in response to eggs in several plant species 12 , 15 , 31 , 32 . We found strong conformable up-regulation of SA-related GS in response to eggs (Fig.…”

Mating Status of an Herbivorous Stink Bug Female Affects the Emission of Oviposition-Induced Plant Volatiles Exploited by an Egg Parasitoid

“…Traces of antiaphrodisiacs were detected into female accessory glands and, when in contact with brassicaceous plants, these compounds induce wax epicuticular changes that arrest Trichogramma egg parasitoids (Fatouros et al, 2009). However, application of antiaphrodisiacs do not fully mimic egg deposition in terms of plant defences, as these compounds do not trigger OIPVs attracting Trichogramma parasitoids (Fatouros et al, 2015). This is similar to our findings, as T. basalis attraction could not be restored when secretions from N. viridula male accessory glands were applied to V. faba plants highlighting the intricacy of plant responses to insect egg deposition.…”