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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.

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