Fragments of ATP synthase mediate plant perception of insect attack

Abstract

Plants can perceive a wide range of biotic attackers and respond with targeted induced defenses. Specificity in plant non-selfrecognition occurs either directly by perception of pest-derived elicitors or indirectly through resistance protein recognition of host targets that are inappropriately proteolyzed. Indirect plant perception can occur during interactions with pathogens, yet evidence for analogous events mediating the detection of insect herbivores remains elusive. Here we report indirect perception of herbivory in cowpea (Vigna unguiculata) plants attacked by fall armyworm (Spodoptera frugiperda) larvae. We isolated and identified a disulfide-bridged peptide ( ؉ ICDINGVCVDA ؊ ), termed inceptin, from S. frugiperda larval oral secretions that promotes cowpea ethylene production at 1 fmol leaf ؊1 and triggers increases in the defenserelated phytohormones salicylic acid and jasmonic acid. Inceptins are proteolytic fragments of chloroplastic ATP synthase ␥-subunit regulatory regions that mediate plant perception of herbivory through the induction of volatile, phenylpropanoid, and protease inhibitor defenses. Only S. frugiperda larvae that previously ingested chloroplastic ATP synthase ␥-subunit proteins and produced inceptins significantly induced cowpea defenses after herbivory. Digestive fragments of an ancient and essential plant enzyme, inceptin functions as a potent indirect signal initiating specific plant responses to insect attack.elicitor ͉ guard hypothesis ͉ indirect perception ͉ insect herbivory ͉ plant defense A mechanistic understanding and targeted improvement of plant resistance traits are recognized as essential in combating yield losses from crop pests. Plants can perceive and defensively respond to attack either directly by impeding pest growth or indirectly by promoting advantageous interactions with beneficial organisms (1-7). Great progress has been made in the identification of plant receptor-like kinase families mediating perception of biotic attack and the subsequent activation of signal transduction cascades spanning interactions of GTP binding proteins, mitogen-activated protein kinases, phytohormones, transcription factors, and ultimately induced biochemical defenses (2,8). Despite these advances, relatively few candidate elicitors and ligands responsible for the initiation and specificity of induced plant defenses to pest attack have been identified (1, 2). This void is especially acute in the case of insect herbivore perception and is surprising given both the significance of plant-insect interactions in arthropod and angiosperm evolution and the role of insects in facilitating plant pathogen entry (9, 10).Induced plant defenses are initiated in part by the direct perception of elicitors derived from offending organisms. For example, maize (Zea mays) and tobacco (Nicotiana attenuata) perceive insect attack through the direct detection of fatty acid amino acid conjugate (FAC) elicitors present in insect oral secretions (OS). Plants respond with indirect defenses in the form of indu...

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

“…A study on volicitin in the regurgitant of Spodoptera exigua showed that the initiation of the response of maize plants to feeding damage was mediated by a protein-ligand interaction in plasma membrane fractions (32). In cowpea, perception of Spodoptera frugiperda herbivory is mediated by fragments of ATP synthase that induce a targeted defense mechanism (27). Interestingly, herbivore saliva is not only able to elicit plant defense but is also able to suppress it (33)(34)(35).…”

“…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).…”

GmPep914, an Eight-Amino Acid Peptide Isolated from Soybean Leaves, Activates Defense-Related Genes

“…Plant endogenous peptide elicitors, systemin (Pearce et al, 1991), HypSys (Pearce et al, 2001a), AtPep (Huffaker et al, 2006), inceptin (Schmelz et al, 2006), GmSubPep (Pearce et al, 2010b), and Gmpep914/890 (this study), were initially purified biochemically using bioassays such as the induction of a defense response or medium alkalinization. These peptides are not similar at the amino acid sequence level, indicating that there will be difficulties elucidating novel endogenous peptide elicitors from databases.…”

“…When cowpea (Vigna unguiculata) leaves were consumed by Spodoptera frugiperda larvae and the oral secretions deposited on the leaves, a proteolyzed fragment of the cowpea chloroplastic ATP synthase produced in the insect gut was found to elicit defense responses (Schmelz et al, 2006). The peptide was termed inceptin and is an example of an indirect signal generated by the insect that initiates specific plant defense responses.…”

Exogenous application of liquid diet, previously fed upon by pea aphidsAcyrthosiphon pisum(Harris), to broad bean leaves induces volatiles attractive to the specialist parasitic waspAphidius ervi(Haliday)

“…Oligosaccharides induce production of defensive compounds under the infection of phytopathogens in the Castor bean, Ricinus commais (Bruce and West 1982). A peptide, inceptin, is one of the elicitors which induce volatile production in Cowpea plants (Schmelz et al 2006). The fraction larger than 3 kDa in molecular weight could contain oligosaccharides and polypeptides.…”