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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.
Highlights
Plants form the base of most terrestrial ecosystems and are under attack by a diverse community of insect herbivores
In comparison to control plants treated with ethanol only, occurrence of hypersensitive response (HR) was significantly higher at low concentration of benzyl cyanide (BC) (0.5 ng/100 μl ethanol; p < 0.008, Bonferroni corrected), but not when the concentration of the chemical was higher (p > 0.05, Figure 3B)
In the present study we show that secretion of accessory reproductive glands (ARGs) of P. brassicae butterflies elicits both a direct (HR-like necrosis) and an indirect defense response in the wild crucifer B. nigra
Summary
Plants form the base of most terrestrial ecosystems and are under attack by a diverse community of insect herbivores. Recognition of more specific effectors in these interactions is based on so-called herbivore-associated molecular patterns (HAMPs), which may be present in, e.g., oral or oviposition secretions (Felton and Tumlinson, 2008; Mithöfer and Boland, 2008; Acevedo et al, 2015; Hilker and Fatouros, 2015). Several effectors like amino acid-lipid conjugates, peptides, or enzymes originating from herbivore salivary glands have been shown to elicit direct plant defenses that can reduce herbivore performance or indirect defenses that improve the foraging of natural enemies (Schoonhoven et al, 2005; Bonaventure et al, 2011; Felton et al, 2014). Relatively little is known on the recognition of HAMPs by plants compared to interactions between plants and microbes, oomycetes, or nematodes, for which hundreds of elicitors have been described (Felton et al, 2014)
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