Armet is an effector protein mediating aphid‐plant interactions

Abstract

Aphid saliva is predicted to contain proteins that modulate plant defenses and facilitate feeding. Armet is a well-characterized bifunctional protein in mammalian systems. Here we report a new role of Armet, namely as an effector protein in the pea aphid, Acyrthosiphon pisum. Pea aphid Armet's physical and chemical properties and its intracellular role are comparable to those reported for mammalian Armets. Uniquely, we detected Armet in aphid watery saliva and in the phloem sap of fava beans fed on by aphids. Armet's transcript level is several times higher in the salivary gland when aphids feed on bean plants than when they feed on an artificial diet. Knockdown of the Armet transcript by RNA interference disturbs aphid feeding behavior on fava beans measured by the electrical penetration graph technique and leads to a shortened life span. Inoculation of pea aphid Armet protein into tobacco leaves induced a transcriptional response that included pathogen-responsive genes. The data suggest that Armet is an effector protein mediating aphid-plant interactions.

Interplay of Plasma Membrane and Vacuolar Ion Channels, Together with BAK1, Elicits Rapid Cytosolic Calcium Elevations in Arabidopsis during Aphid Feeding

“…As a result, there is no capacity to increase plant susceptibility to the aphid by disrupting Ca 2+ signaling. The suppression of Arabidopsis defense by aphids is achieved via effector proteins (Bos et al, 2010;Hogenhout and Bos, 2011;Pitino and Hogenhout, 2013;Atamian et al, 2013;Elzinga et al, 2014;Naessens et al, 2015;Wang et al, 2015;Kettles and Kaloshian, 2016) that are injected into epidermal and mesophyll cells during feeding (Martín et al, 1997;Moreno et al, 2011;Mugford et al, 2016). These effectors may actively suppress the feeding site [Ca 2+ ] cyt elevations, as aphid saliva contains Ca 2+ binding proteins Carolan et al, 2009;Rao et al, 2013).…”

“…Indeed, aphid saliva contains Ca 2+ binding proteins Carolan et al, 2009;Rao et al, 2013), and application of saliva to legume phloemplugging proteins results in their contraction . Aphid saliva also contains effector molecules that suppress plant defense (Bos et al, 2010;Pitino and Hogenhout, 2013;Atamian et al, 2013;Naessens et al, 2015;Wang et al, 2015;Kettles and Kaloshian, 2016), as observed with microbial pathogens (Jones and Dangl, 2006;Galán et al, 2014) and chewing insects (Musser et al, 2002).…”

The Salivary Protein Repertoire of the Polyphagous Spider Mite Tetranychus urticae: A Quest for Effectors

“…for salivary proteins-such as effectors-has been reported for aphids as well (108,110,129). Elzinga et al (129) suggested that the differential expression of salivary effector genes represents a strategy to avoid activation of defenses and to facilitate feeding.…”

A Salivary Endo-β-1,4-Glucanase Acts as an Effector That Enables the Brown Planthopper to Feed on Rice

“…Expressing C002 from the green peach aphid Myzus persicae in Nicotiana benthamiana increased aphid reproduction on these plants, whereas reducing C002 expression in aphids by plant-mediated RNA interference (RNAi) reduced aphid fecundity (Bos et al, 2010;Pitino et al, 2011). Other salivary proteins, such as Glc oxidase from the corn earworm Helicoverpa zea (Musser et al, 2002), calcium-binding proteins from the vetch aphid Megoura viciae (Will et al, 2007), Mp10 and Mp55 from the green peach aphid (Bos et al, 2010;Elzinga et al, 2014), structural sheath proteins from the grain aphid Sitobion avenae (Abdellatef et al, 2015), Me10 and Me23 from the potato aphid Macrosiphum euphorbiae (Atamian et al, 2013), and Armet from the pea aphid (Wang et al, 2015), also have been found to increase herbivore performance. Thus, herbivore effectors play a central role in overcoming plant defenses and helping the herbivore establish a population on host plants.…”