Cowpea Chloroplastic ATP Synthase Is the Source of Multiple Plant Defense Elicitors during Insect Herbivory

Schmelz, Eric A.; LeClere, Sherry; Carroll, Mark J.; Alborn, Hans T.; Teal, Peter E. A.

doi:10.1104/pp.107.097154

Cited by 135 publications

(102 citation statements)

References 83 publications

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“…In summary, we interpret the phylogenically idiosyncratic nature of elicitor action as additional indirect evidence for the existence of volicitin and inceptin receptors in maize and cowpea, respectively, and although little is known about caeliferins, modern tools for genetic mapping, microarray, and mutant analyses will expedite future discoveries (11,18,35,44).…”

Section: Discussionmentioning

confidence: 88%

“…Likewise, the inactivity of FACs in A. thaliana, cowpea, and tomato argues against relatively non-specific pore-formation mechanisms and supports plant recognition mediated by specific binding proteins (39,41). ln contrast to FACs, inceptin represents a seemingly uncommon divergence from direct plant recognition of an insect-synthesized elicitor to an indirect recognition system based on insect catabolism (14,18,53).…”

Section: Discussionmentioning

confidence: 97%

“…Unlike maize, lima bean (Phaseolus lunatus) and cotton (Gossypium hirsutum) do not exhibit rapid volicitin-induced VOCs, suggesting that FACs are not ''general elicitors'' of induced plant responses (17). To understand the lack of FAC activity in legumes, the phytohormone ethylene (E) was used as an inducible marker in cowpea (Vigna unguiculata) to guide the chemical fractionation of Spodoptera frugiperda larval OS and resulted in the isolation of chloroplastic ATP synthase ␥-subunit-derived peptide elicitors termed inceptins (14,18). More recently, a maize VOC bioassay was again used to monitor the chemical isolation of grasshopper (Schistocerca americana) OS elicitors and resulted in the identification of a complex mixture of disulfo-oxy fatty acids, termed caeliferins (11).…”

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confidence: 99%

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Phytohormone-based activity mapping of insect herbivore-produced elicitors

Schmelz

Engelberth

Alborn

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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233

225

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In response to insect attack, many plants exhibit dynamic biochemical changes, resulting in the induced production of direct and indirect defenses. Elicitors present in herbivore oral secretions are believed to positively regulate many inducible plant defenses; however, little is known about the specificity of elicitor recognition in plants. To investigate the phylogenic distribution of elicitor activity, we tested representatives from three different elicitor classes on the time course of defense-related phytohormone production, including ethylene (E), jasmonic acid (JA), and salicylic acid, in a range of plant species spanning angiosperm diversity. All families examined responded to at least one elicitor class with significant increases in E and JA production within 1 to 2 h after treatment, yet elicitation activity among species was highly idiosyncratic. The fatty-acid amino acid conjugate volicitin exhibited the widest range of phytohormone and volatile inducing activity, which spanned maize (Zea mays), soybean (Glycine max), and eggplant (Solanum melongena). In contrast, the activity of inceptinrelated peptides, originally described in cowpea (Vigna unguiculata), was limited even within the Fabaceae. Similarly, caeliferin A16:0, a disulfooxy fatty acid from grasshoppers, was the only elicitor with demonstrable activity in Arabidopsis thaliana. Although precise mechanisms remain unknown, the unpredictable nature of elicitor activity between plant species supports the existence of specific receptor-ligand interactions mediating recognition. Despite the lack of an ideal plant model for studying the action of numerous elicitors, E and JA exist as highly conserved and readily quantifiable markers for future discoveries in this field.ethylene ͉ insect elicitor ͉ jasmonic acid ͉ plant defense ͉ volatile organic compound

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Section: Discussionmentioning

confidence: 88%

Section: Discussionmentioning

confidence: 97%

mentioning

confidence: 99%

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Phytohormone-based activity mapping of insect herbivore-produced elicitors

Schmelz

Engelberth

Alborn

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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233

225

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“…The chemical nature of a few elicitors of feeding-induced plant defense responses are known: fatty acid-amino acid conjugates, including volicitin, of several lepidopterans (6,7,(23)(24)(25)(26); peptides derived by proteolysis from chloroplastic ATP synthase of herbivore-damaged plants (27,28); disulfo-oxy fatty acids of grasshopper regurgitant, named caeliferins (29); and the enzyme ␤-glucosidase from Pieris brassicae oral secretions (8). Application of these elicitors onto plant wounds results in the release of volatiles that repel ovipositing herbivores (30) or attract natural enemies of herbivores (31).…”

Section: Discussionmentioning

confidence: 99%

Male-derived butterfly anti-aphrodisiac mediates induced indirect plant defense

Fatouros¹,

Broekgaarden

Bukovinszkine’Kiss³

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

112

106

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Plants can recruit parasitic wasps in response to egg deposition by herbivorous insects-a sophisticated indirect plant defense mechanism. Oviposition by the Large Cabbage White butterfly Pieris brassicae on Brussels sprout plants induces phytochemical changes that arrest the egg parasitoid Trichogramma brassicae. Here, we report the identification of an elicitor of such an ovipositioninduced plant response. Eliciting activity was present in accessory gland secretions released by mated female butterflies during egg deposition. In contrast, gland secretions from virgin female butterflies were inactive. In the male ejaculate, P. brassicae females receive the anti-aphrodisiac benzyl cyanide (BC) that reduces the females' attractiveness for subsequent mating. We detected this pheromone in the accessory gland secretion released by mated female butterflies. When applied onto leaves, BC alone induced phytochemical changes that arrested females of the egg parasitoid. Microarray analyses revealed a similarity in induced plant responses that may explain the arrest of T. brassicae to egg-laden and BC-treated plants. Thus, a male-derived compound endangers the offspring of the butterfly by inducing plant defense. Recently, BC was shown to play a role in foraging behavior of T. brassicae, by acting as a cue to facilitate phoretic transport by mated female butterflies to oviposition sites. Our results suggest that the antiaphrodisiac pheromone incurs fitness costs for the butterfly by both mediating phoretic behavior and inducing plant defense.egg parasitoid ͉ elicitor ͉ Trichogramma brassicae ͉ Pieris brassicae ͉ Brussels sprouts C hemical signals play a crucial role in the interactions between herbivorous insects and parasitic wasps (1). To locate the tiny eggs of herbivorous host insects in an 'ocean' of plant biomass, egg parasitoids have been shown to employ chemical cues either induced in the plant by host egg deposition or from the adult host stage [i.e., infochemical detour, (2)], whereas only short-range cues emanate from the eggs themselves (3). Plants injured by feeding herbivores often start to release chemical cues that attract predators and parasitoids to effectively defend the plant by killing the herbivores (4, 5). This indirect plant defense may be triggered by compounds in the regurgitant of the herbivore, allowing the plant to discriminate between mechanical wounding and insect feeding (6-8). Plants can also respond before being damaged by insect feeding. Egg deposition by herbivorous insects induces volatiles attractive to egg parasitoids in tritrophic interactions associated with elm, pine, and bean plants (9). The elicitor of these oviposition-induced parasitoid attractants (synomones) was shown to be located in the oviduct secretion of the female herbivore, which is used to glue eggs onto leaves (10,11).Recent data revealed that egg deposition by Pieris brassicae on Brussels sprouts plants (Brassica oleracea var. gemmifera cv. Cyrus) induces chemical changes in the leaf surface that arrest the egg parasi...

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“…Moreover, it has been demonstrated that specific Lepidopteran oral secretion elicitors can be used to predict elicitation of legume defense responses following natural bouts of herbivory (Schmelz et al 2006(Schmelz et al , 2012. First identified from beet armyworm S. exigua larvae, fatty acid-amino acid conjugates (FACs) remain the most extensively examined insect-produced elicitors (Alborn et al 1997).…”

Section: Introductionmentioning

confidence: 99%

Inducible De Novo Biosynthesis of Isoflavonoids in Soybean Leaves by Spodoptera litura Derived Elicitors: Tracer Techniques Aided by High Resolution LCMS

et al. 2016

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Isoflavonoids are a characteristic family of natural products in legumes known to mediate a range of plant-biotic interactions. For example, in soybean (Glycine max: Fabaceae) multiple isoflavones are induced and accumulate in leaves following attack by Spodoptera litura (Lepidoptera: Noctuidae) larvae. To quantitatively examine patterns of activated de novo biosynthesis, soybean (Var. Enrei) leaves were treated with a combination of plant defense elicitors present in S. litura gut content extracts and L-α-[ 13 C 9 , 15 N]phenylalanine as a traceable isoflavonoid precursor. Combined treatments promoted significant increases in 13 Clabeled isoflavone aglycones (daidzein, formononetin, and genistein), 13 C-labeled isoflavone 7-O-glucosides (daidzin, ononin, and genistin), and 13 C-labeled isoflavone 7-O-(6″-O-malonyl-β-glucosides) (malonyldaidzin, malonylononin, and malonylgenistin). In contrast levels of 13 C-labeled flavones and flavonol (4′,7-dihydroxyflavone, kaempferol, and apigenin) were not significantly altered. Curiously, application of fatty acid-amino acid conjugate (FAC) elicitors present in S. litura gut contents, namely N-linolenoyl-L-glutamine and N-linoleoyl-L-glutamine, both promoted the induced accumulation of isoflavone 7-O-glucosides and isoflavone 7-O-(6″-O-malonyl-β-glucosides), but not isoflavone aglycones in the leaves. These results demonstrate that at least two separate reactions are involved in elicitor-induced soybean leaf responses to the S. litura gut contents: one is the de novo biosynthesis of isoflavone conjugates induced by FACs, and the other is the hydrolysis of the isoflavone conjugates to yield isoflavone aglycones. Gut content extracts alone displayed no hydrolytic activity. The quantitative analysis of isoflavone de novo biosynthesis, with respect to both aglycones and conjugates, affords a useful bioassay system for the discovery of additional plant defense elicitor(s) in S. litura gut contents that specifically promote hydrolysis of isoflavone conjugates.

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Cowpea Chloroplastic ATP Synthase Is the Source of Multiple Plant Defense Elicitors during Insect Herbivory

Cited by 135 publications

References 83 publications

Phytohormone-based activity mapping of insect herbivore-produced elicitors

Phytohormone-based activity mapping of insect herbivore-produced elicitors

Male-derived butterfly anti-aphrodisiac mediates induced indirect plant defense

Inducible De Novo Biosynthesis of Isoflavonoids in Soybean Leaves by Spodoptera litura Derived Elicitors: Tracer Techniques Aided by High Resolution LCMS

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